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Full text of "Properties of temporomandibular joint nociceptors in normal and inflamed tissue"

PROPERTIES OF TEMPOROMANDIBULAR JOINT NOCICEPTORS 
IN NORMAL AND INFLAMED TISSUE 



\ 



BY 



BARRY LOUGHNER 



A DISSERTATION PRESENTED TO THE GRADUATE SCHOOL 

OF THE UNIVERSITY OF FLORIDA IN PARTIAL FULFILLMENT 

OF THE REQUIREMENTS FOR THE DEGREE OF 

DOCTOR OF PHILOSOPHY 



UNIVERSITY OF FLORIDA 
1992 



I dedicate this work to my daughter. Carina Beth. 



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ACKNOWLEDGEMENTS 

I thank Dr. Brian Cooper, Ph.D., for his technical guidance in the research 
involved in this dissertation. I thank Ms. Martha Oberdorfer for her technical assistance. I 
thank Dr. Parker Mahan, D.D.S., Ph.D., and Dr. Arnold S. Bleiweis, Ph.D. for their 
strategic guidance. I thank Dr. Robert Bates, D.D.S., M.S. for his administrative 
assistance. 






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TABLE OF CONTENTS ** ' ' ' 



LIST OF TABLES vi 

LIST OF FIGURES ...! viii 

KEY TO SYMBOLS ix 

ABSTRACT x 

CHAPTERS 

1 INTRODUCTION 1 

2 METHODS 4 

Subjects 4 

Exposure of the TMJ and Trigeminal Ganglion 4 

Recording Procedures 5 

Characterization of TMJ Afferents 6 

Statistics 11 

Experimental Inflammation 13 

3 RESULTS 16 

Identification of TMJ Nociceptors 16 

Characterization of TMJ Nociceptors in Normal Tissue 21 

f*roperties of TMJ Nociceptors in Inflamed Tissue 27 

Experiment I: Properties of units in the Previously Inflamed TMJ ... 31 

Experiment II: Properties of Units in the Acutely Inflamed TMJ 36 

4 DISCUSSION 52 

Sensitization of TMJ Nociceptors 54 

Factors Contributing to Sensitization 57 

APPENDICES 

A DEVELOPMENT AND MAINTENANCE OF TMJ PAIN 60 

B PSYCHOPHYSICS OF TMJ DISORDERS 67 

C NEUROANATOMY OF THE TMJ 75 

D CENTRAL REPRESENTATION OF TMJ AFFERENTS 81 

E TRIGEMINAL GANGLION 84 

F GROSSANATOMY 86 



IV 



G SUMMARY TABLES OF TMJ REACTIVITY 90 

LIST OF REFERENCES 118 

BIOGRAPHICAL SKETCH 130 



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LIST OF TABLES 

Table 3-1 TMJ force/movement relationships in the vertical plane 25 

Table 3-2 Properties on nociceptors that demonstrate vertical plane or horizontal 

plane reactivity 28 

Table 3-3 Mean values of properties of TMJ nociceptors 37 

Table 3-4 Qualitative improvements in reactivity for nociceptors that were 
characterized in normal tissue and then tested again subsequent to 

carrageenan injection 46 

Table 3-5 Changes in reactivity for 8 units after exposure to saline 51 

TableG-1 Reactivity in vertical plane (normal tissue) 91 

Table G-2 Reactivity in horizontal plane (normal tissue), left lateral 92 

Table G-3 Reactivity in horizontal plane (normal tissue), right lateral 93 

Table G-4 Reactivity in the vertical plane in previously inflamed tissue. Reactivity 

in horizontal plane in previously inflamed tissue, left lateral 94 

Table G-5 TMJ nociceptor reactivity in normal tissue, vertical plane 95 

Table G-6 TMJ nociceptor reactivity in normal tissue, horizontal plane 96 

Table G-7 TMJ nociceptor reactivity in previously inflamed tissue 97 

Table G-8 TMJ nociceptor reactivity in acutely inflamed tissue 98 

Table G-9 TMJ nociceptor reactivity in saline injected tissue 99 

Table G-10 Effect of carrageenan in acutely inflamed tissue reactivity in the vertical 

plane, unit #1 I(X) 

Table G-11 Effect of carrageenan in acutely inflamed tissue reactivity in the vertical 

plane, unit #2 101 

Table G-12 Effect of carrageenan in acutely inflamed tissue reactivity in the vertical 

plane, unit #3 102 

Table G- 1 3 Effect of carrageenan in acutely inflamed tissue reactivity in the vertical 

plane, unit #4 103 



vi 



* 



Table G- 14 Effect of carrageenan in acutely inflamed tissue reactivity in the horizontal 

plane,unit#l 104 

Table G- 1 5 Effect of carrageenan in acutely inflamed tissue reactivity in the horizontal 

plane,unit#2 105 

Table G- 16 Effect of carrageenan in acutely inflamed tissue reactivity in the horizontal 

plane,unit#3 106 

Table G-17 Effect of carrageenan in acutely inflamed tissue reactivity in the horizontal 

plane,unit#4 107 

Table G- 1 8 Effect of carrageenan in acutely inflamed tissue reactivity in the horizontal 

plane,unit#5 108 

Table G-19 Effect of carrageenan in acutely inflamed tissue reactivity in the horizontal 

plane,unit#6 109 

Table G-20 Effect of carrageenan in acutely inflamed tissue reactivity in the horizontal 

plane, unit #7 110 

Table G-21 Effect of saline reactivity in the horizontal plane, unit #1 Ill 

Table G-22 Effect of saline reactivity in the horizontal plane, unit #2 112 

Table G-23 Effect of saline reactivity in the horizontal plane, unit #3 113 

Table G-24 Effect of saline reactivity in the horizontal plane, unit #4 114 

Table G-25 Effect of saline reactivity in the horizontal plane, unit #6 115 

Table G-26 Effect of saline reactivity in the horizontal plane, unit #7 116 

Table G-27 Effect of saline reactivity in the horizontal plane, unit #8 117 



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- LIST OF FIGURES ^ ■■ ' 

Figure 2- 1 Mandibular movements were produced by a hand held probe 8 

Figure 2-2 Dynamic and static test series for force, displacement and velocity 10 

Figure 2-3 Demonstration of sensitization as a shift of stimulus-response functions.. 14 

Figure 3- 1 Receptive field distribution in the lateral and posterior capsule of the 

temporomandibular joint for normal tissue 18 

Figure 3-2 Receptive field distribution in the lateral and posterior capsule of 

the temporomandibular joint for previously inflamed tissue, acutely 
inflamed tissue and saline control tissue 20 

Figure 3-3 Relationships between applied force and vertical plane movements of 

the mandible 23-24 

Figure 3-4 Dynamic reactivity in normal tissue 30 

Figure 3-5 Dynamic reactivity in previously inflamed tissue 33 

Figure 3-6 Averaged dynamic response functions of nociceptors fitted in normal 

and previously inflamed tissue 41 

Figure 3-8 Reactivity of nociceptors exposed to saline 43 

Figure 3-9 Comparison between pre-inflamed and post-inflamed reactivity in 

scatter plot forms 48-49 

Figure F-1 Schematic diagram of the human temporomandibular joint. Sagittal and 

frontal views 87 



vin 



KEY TO SYMBOLS 
• Vertical plane or previously inflamed tisue. 

A Horizontal plane or acutely inflamed tissue. 

+ Saline control tissue. 



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IX 



Abstract of Dissertation Presented to the Graduate School 

of the University of Florida in Partial Fulfillment of the 

Requirements for the Degree of Doctor of Philosophy 

PROPERTIES OF TEMPOROMANDIBULAR JOINT NOCICEPTORS 
IN NORMAL AND INFLAMED TISSUE 

By . 

Barry Loughner 

" May, 1992 



Chairman: Parker Mahan, D.D.S., Ph.D. 

Cochairman: Brian Cooper, Ph.D. ^ 

Major Department: Oral Biology 

Mechanical response properties of nociceptors of the goat temporomandibular joint 
(TMJ) were characterized by unit recordings from the trigeminal ganglion. Populations of 
afferents were sampled in normal tissue and in tissue previously inflamed (PI) with 
carrageenan for at least 6 hours prior to testing. In other experiments, nociceptors were 
characterized in normal tissue and then retested for up to 3 hrs subsequent to exposure to 
carrageenan (AI). To produce mandibular movement in the vertical and horizontal planes, 
dynamic and static forces were applied to the mandibular pole. Stimuli were quantified by 
force and angular displacement transducers. Receptive fields were small, single spots (2-3 
mm) and located on the lateral or posterior capsule of the TMJ. Conduction velocities were 
shown to be in the group III and IV range. Stimulus-interval data was best described by 
power functions. Assessment of force-movement relationships indicated that capsular 
nociceptors responded exclusively to intense forces that produce extreme displacements of 
the mandible. 



In normal tissue, 24 of 36 nociceptors transduced dynamically applied stimuli 
(mean activation threshold for dynamic force = 15.9 ± 11.3 N and for force velocity = 
17.3 ± 18.9 N/s). Relatively fewer units transduced static force (8/36) or position 
(1/36). - 

In PI conditions, tests revealed enhanced reactivity for dynamically applied 
stimuli. Mean power functions for dynamic tests in PI conditions (LnlSI = -1.3 LnF + 
7.3) had steeper slopes compared to those in normal tissue (LnlSI = -1.1 LnF + 5.4) 
and were shifted graphically to regions indicating greater reactivity (below and to the 
left of those in normal tissue). These shifts were suggestive of sensitization. 

In AI conditions, 8 of 1 1 nociceptors acquired either dynamic or static coding 
ability. Acquired coding ability also appeared in nociceptors (n = 2) that were without 
transducing capacity in normal tissue. Acquired reactivity for vertical plane movement 
was also seen for those nociceptors (n = 3) that were reactive only to movement in the 
horizontal plane in normal tissue. Acquisition of coding ability followdng carrageenan- 
induced inflammation suggested afferent sensitization. 



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CHAPTER 1 



INTRODUCTION 



The temporomandibular joint (TMJ) is the site of a number of disorders that burden 
the health care system and extract a large cost in human suffering (Helkimo, 1979; Solberg, 
1987). Afferent groups presumed to mediate TMJ pain are likely to play a role in a variety 
of TMJ disorders. Many theories have been proposed to explain TMJ pain and dysfunction 
(Deboever, 1973; Dubner et al., 1978, Yemm, 1979). These theories propose both intra- 
and extra-articular origins of TMJ pain. Intra-articular theories argue that pressure or 
tension on articular tissues results in TMJ pain. Extra-articular theories propose that 
muscles or other contiguous structures refer pain to the TMJ (see Appendix A). 
Fundamental to an evaluation of intra-articular theories is an understanding of the response 
properties of TMJ nociceptors. 

Our understanding of nociceptors innervating articular tissues has been advanced in 
recent years (Schaible and Schmidt, 1983a, b, 1988b; Guilbaud et al., 1985; Birrell et al., 
1990). Most detailed information concerning the response properties of joint nociceptors 
has come from studies of the cat knee and rat ankle joint. While there is considerable 
information regarding the neuroanatomy of the TMJ (see Appendix C), little is known 
about the physiology of nociceptors of the temporomandibular joint. 

Early studies examining properties of afferents innervating the cat knee joint 
reported activation of slowly conducting, myelinated fibers only by forceful rotational 
movements beyond the physiological range of motion (Burgess and Clark, 1969; Clark and 
Burgess, 1975). In contrast, Schaible and Schmidt (1983b) identified populations of 



small fibers that were activated by passive movement of the knee joint, both within and 
beyond the normal range of motion. These afferents were categorized into four populations 
on the basis of their response range. Afferents of populations 1 and II responded to 
innocuous joint movement in the normal range of motion, but population II responded best 
to forceful rotation. Population III units were activated exclusively by forceful movement 
and population IV had no response to movement. Based on movement sensitivity, 
afferents that responded within the normal range of motion were not considered 
nociceptors, while those that respond beyond the normal range were nociceptors. 
Subsequent studies by Schaible and Schmidt (1985, 1988b) concentrated on populations 
ni and IV. However, despite the imponance of range for classifying afferents, distinctions 
between normal and non-normal ranges have been ancedotal. Quantification of the 
relationship between range of motion and afferent activity is still pending. 

There are no studies that have examined properties of TMJ nociceptors. Previous 
reports have examined the discharge characteristics of afferent traffic in the 
auriculotemporal nerve that may contribute to position sense and control of mandibular 
movement (Kawamura et al., 1967; Klineberg et al, 1970, 1971; Kawamura and Abe, 
1974; Lund and Matthews, 1981). While TMJ nociceptors may have properties similar to 
those described for cat knee joint, there are considerable functional and anatomical 
differences between these two joints that indicate that properties of TMJ nociceptors should 
be determined (see Appendices C and F). 

Changes in the properties of TMJ nociceptors (sensitization) may account for some 
of the symptoms of TMJ dysfunction. These symptoms include pain during mandibular 
movement, pain on local joint palpation, and tonic pain. Changes in nociceptor properties 
are likely to be necessary to the development of these forms of pain. As pain on movement 
is a primary symptom of TMJ dysfunction, a precise determination of the relationship 
between movement and afferent discharges is valuable. Quantification of force and 
movement also permits more direct specifications of movements which are outside the 



normal range of motion, and identification of afferents that respond specifically in these 
ranges. 

Sensitization of TMJ receptors may be an important defense mechanism that 
protects the joint from excessive movement which may cause injury. The TMJ is often the 
site of inflammations associated with various forms of TMJ dysfunction (e.g. arthritis and 
synovitis). An understanding of how inflammation may modify TMJ afferent function 
would reveal the form and range of TMJ afferent sensitization and lead to a better 
understanding of both etiology and treatment. 

Sensitization of nociceptors has been documented in the cat knee joint (Coggeshall 
et al., 1983; Schaible and Schmidt, 1985, 1988b; Grigg et al., 1986) and in the rat ankle 
joint (Guilbaud et al., 1985) following chemically-induced acute or chronic arthritis. Acute 
arthritis in the cat knee joint, induced by carrageenan and kaolin, produced changes in the 
discharge properties in joint afferents. These changes include an increase in the proportion 
of small fibers that could be activated by innocuous joint movement, recruited units, and 
the appearance of spontaneous activity. Studies of sensitization of TMJ nociceptors may 
provide uniquely important information regarding short and long term changes occurring in 
TMJ afferents following local trauma, arthritis or chronic disc displacement. 

In the following experiments, we examined properties of TMJ nociceptors in both 
normal and inflamed tissue of the goat. The goat is an excellent model for TMJ physiology 
because of functional and structural similarities to humans including range of motion and 
innervation of the auriculotemporal nerve. (See Appendices C and F). 



^ ■':> ^ W 



CHAPTER 2 



METHODS 



- ' Subjects 

Experiments were performed on 59 goats, ages 6-12 months and weighing 30-60 
lbs. All goats were kept in pens at the veterinary hospital. Goat health was monitored and 
maintained by animal care technicians, veterinary staff and faculty. All procedures were 
approved by an internal review board (protocol 7136). 

Exposure of the TMJ and Trigeminal Ganglion 

Rompun (3 mg/kg) and Ketamine (11 mg/kg) were given as preanesthetics. 
Anesthesia was induced with a-chloralose (7.5 mg/ml) via a lactated ringers drip. If 
necessary, pentabarbitol was periodically administered intravenously to maintain deep 
anesthesia. Goats were artifically respirated at a rate of 10-20 breaths per minute. Blood 
pressure, body temperature and end-tidal CO2 were continuously monitored and maintained 
within physiological limits. At the conclusion of each experiment, the goats were 
euthanized with saturated KCL. 

To expose the right TMJ, the skin was removed from the lateral posterior aspect of 
the face. The parotid gland, pinna and the zygomaticoauricularis muscles were removed to 
access the posterior portion of the TMJ capsule. The styloid process and associated 
muscular and ligamentous attachments were clipped off at the sphenoid bone. The origin of 



the stemomastoid and caudal digastric muscles were excised from the mastoid process and 
jugular process of the occiput, respectively. The sphenomandibular ligament and fatty 
tissues were removed. Care was taken to preserve the microvasculature of the TMJ 
capsule. The exposed capsular tissue was kept moist by repeated applications of 
physiological saline. 

Several nerves were cut distal to the trigeminal ganglion in order to avoid recording 
activity other than TMJ afferents. The buccinator nerve was severed as it passed the 
anterior border of the masseter muscle. The masseteric nerve was cut as it entered the deep 
and superficial masseter muscle. The posterior trunk of the mandibular nerve was cut distal 
to the branching of the auriculotemporal nerve. As a consequence, afferents of the lingual, 
inferior alveolar and mylohyoid nerves were eliminated. 

The trigeminal ganglion was accessed via its position caudal to the foramen ovale. 
Removal of the thin, lateral plate of bone of the tympanic bulla and the tympanic plate 
exposed the ossicles of the middle ear and internal surface of the tympanic membrane. 
Removal of the inferior aspect of the greater wing of the sphenoid and the inferior aspect of 
the petrous bone exposed the caudal surace of the trigeminal ganglion. Access to the 
ganglion is improved by removing the sphenomandibular ligament and fatty tissue in the 
infratemporal fossa. ^ 

Recording Procedures 

Extracellular recordings were made by penetration of the trigeminal ganglion with 
tungsten microelectrodes (Microprobe, Inc.) until unit potentials were evoked by passive 
jaw movement. Most units were found in the posterior region of the trigeminal ganglion. 
(See Appendix E). Receptive fields were then identified on the lateral or posterior capsule 
of the TMJ. Amplified output was led to and monitored by a digital oscilloscof)e and an 
audio speaker. Data was digitized and stored on video tape (Vetter Instruments, Model No. 



3000A). Data were recovered from tape for analysis with an RC computerscope (RC 
Electronics) or captured on a line by a thermal printer (Astromed, Dash IV). 

After a unit was characterized, the conduction velocity was determined by 
measuring the latency of resp>onses to suprathreshold electrical stimulation applied to the 
receptive field on the TMJ capsule. Electrical stimulation was performed with a Grass S88 
stimulator and isolated, constant current unit. Square-wave pulses of 0.2 to 2 msec 
duration were applied with monopolar electrodes. Conduction distance was estimated in 
situ. '■■-'■<■■ 

Characterization of TMJ Afferents 

Once an afferent was isolated, passive jaw movements were used to determine 
which type of movement was preferred (preferred movements were those which produced 
the most vigorous response). Jaw movements included: 1) vertical jaw movements from 
the closed to the open position. Afferent responses to vertical jaw movements were termed 
"vertical plane reactivity" (VP); 2) lateral jaw movements from the closed to extreme lateral 
position. Afferent responses to the lateral jaw movements were termed "horizontal plane 
reactivity" (HP). 

A force probe was used to produce jaw movement. The probe consisted of an axial 
force transducer (Entran Instruments, Model ELF TC500-20) embedded in a plexiglass 
rod. The transducer monitored forces used to move the jaw in the vertical or horizontal 
plane. The probe was applied to fixed points of a bit which was mounted to the incisal 
teeth of the mandible at the midline. Force and jaw movement were recorded on video tape 
along with afferent activity. Jaw movement was monitored by an angular displacement 
transducer (ADT, Trans-Tek Model # 604-001) mounted above the right TMJ (Figure 2-1). 
Using the probe, both dynamic and static forces were applied to the mandible (Figure 2-2). 



-% ;■ 






Figure 2-1. Mandibular movements were produced by a hand held probe. Force 
applied to the mandible was quantified by a force transducer. Vertical 
plane mandibular movement was quantified by an angular displacement 
transducer mounted above the right TMJ and attached to the mandibular 
pole by a slide assembly. Vertical plane movement of the mandible was 
produced by applying force at point A on the jaw movement apparatus. 
Horizontal plane movement was produced by applying force at point B. 
Afferent recordings were made following exposure and penetration of the 
trigeminal ganglion proximal to the foramen ovale. 



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Angular 

Displacement 

Transducer 




Oscilloscope 







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Figure 2-2. Dynamic and static test series for force, displacement and velocity. A) 
Dynamic test series. Sawtooth patterns of successively increasing 
velocities. B) Static test series. Stepwise pattern of successively 
increasing force and displacement. > ■ 



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TEST FOR DYNAMIC REACTIVITY 



UNITS 



FORCE (N) 



DISPLACEMENT (d^) 




TIME 



B 



TEST FOR STATIC REACTIVITY 



UNTTS 



H ^ !h 



HI- 



FORCE (N) 



10 



DISPLACEMENT (d«g) 



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11 



Isolated units were characterized by two series of jaw manipulations. The first 
series consisted of five tests of reactivity to dynamic force. The first, at a low velocity, 
was followed by jaw movements of progressively higher velocities. The range of 
velocities was approximately 0.3 to 250.0 N/sec. The second series consisted of five 
stepwise, static force applications. Each step was maintained for approximately 2 seconds. 
Forces up to 120 N were applied. '.-'-■ 

To confirm that jaw movement activated afferents of the TMJ capsule, receptive 
fields on the capsule were identified and characterized for each case. Thresholds for 
activation of mechanosensitive afferents on the capsule of the TMJ were determined by the 
bending force of von Frey filaments (monofilament nylon) of different stiffnesses. The 
method of limits was used to determine threshold. Nylon probes were applied to the 
capsular field until the minimum force required to activate the afferent was determined. In 
some cases, no receptive field could be found. This group of cases was treated separately 
from afferents with identified receptive fields. 

Statistics 

Nociceptors were defined as those afferents that responded preferentially to 
extremes of jaw movement. Relationships between force applied and jaw movement were 
assessed to determine whether the afferents reacted at movement extremes. Force- 
movement data was plotted for all units (n = 10) that responded preferentially to vertical 
jaw movement and produced significant functions. Momentary relationships between 
force, jaw movement and unit activity were determined. Force-interspike interval, 
movement-interspike interval and velocity-interspike interval records were fit to linear, 
logarithmic, exponential or power functions using simple linear regression (Statistical 
Analysis System, SAS). The best fits were determined by comparison of coefficients of 
determination. 



12 



For analysis of static reactivity, regression data were "segmented and balanced." A 
segment (or step) of force was added to tiie regression model until the coefficient of 
determination was maximal. The regression was "balanced" by using only six scores for 
each stepwise force segment. This procedure avoids weighting the regression differentially 
at higher steps, where more scores typically bias the regression. These procedures were 
not possible on tests of dynamic force reactivity. Therefore, for dynamic force or 
movement tests, all spike intervals were used until a minimum interval was obtained. 

Several characteristics of regression lines were subjected to analysis. These 
included force-activation thresholds, movement-activation thresholds, force-frequency 
asymptotes, movement-frequency asymptotes, mean response intervals, slopes and 
intercepts. Force-activation thresholds (FAT) and movement-activation thresholds (MAT) 
were defined as the instantaneous force or degree of movement at the first response 
interval. Force-frequency asymptotes (FFA) and movement-frequency asymptotes (MFA) 
were defined as the force or movement at which the frequency response was maximal (i.e., 
minimum response interval). The FAT or MAT paired with the FFA or FMA were used as 
the lower and upper boundary values to plot functions derived from regressions. The mean 
response interval (MRI) was calculated from the regression equation by using the mean 
force or movement value calculated from the boundary values (FAT -i- FFA/2 or MAT + 
MFA/2). Force-frequency thresholds and movement-frequency thresholds (FFTs and 
MFTs) were determined for each unit that was tested for static reactivity. The FFT and 
MFT were defined as the minimum force or movement which would maintain a sustained 
discharge of the afferent. Slopes, intercepts and coefficients of determination were 
generated only from significant regressions. Unit reactivity that could not be described by 
significant functions were called "non-coding" or "non-transducing" afferents. 

"Sensitization" refers to the enhanced excitability of TMJ afferents that may occur 
following carrageenan-induced inflammation. Enhanced excitability is reflected 
quantitatively as changes in resix)nse propenies of TMJ afferents in normal and in inflamed 



-»^'"-^'- 



13 



tissue. Sensitization was assessed qualitatively by comparisons of functions fit to units in 
normal and inflamed tissues. 

Shifts of stimulus-response coding functions were used as an indication of 
enhanced reactivity. Significant functions generated from responses of afferents in 
inflamed tissue that were located graphically below and/or to the left of functions fit in 
normal tissue were suggestive of sensitization (See Figure 2-3). Significant functions that 
were acquired in inflamed tissue but not expressed in normal tissue also were considered to 
represent sensitization. Sensitization was assessed quantitatively by statistical comparisons 
of function characteristics generated from stimulus tests on units in normal and inflamed 
conditions. Function characteristics (slope, intercept, thresholds, asymptotic activity, 
coefficients of determination and mean interval) were compared in normal and inflamed 
conditions using a one-way ANOVA (Li, 1967) for between subject and t-tests for within 
subject's comparisons. Only significant functions contributed to the analysis. 

Experimental Inflammation - - . 

Inflammation of the TMJ was induced by injection of 200 ^il of 2% carrageenan 
(Sigma Chem.). In some cases, units were characterized in normal tissue and then exposed 
to carrageenan. If the receptive field was located on the lateral side of the capsule, 
carrageenan was dropped directly onto the receptive field as well as injected into the area of 
the receptive field. If the receptive field was located on the posterior side of the capsule, 
carrageenan was injected into the area of the receptive field. The remainder of the 
carrageenan was injected into the superior joint space. Subsequent testing was performed 
after at least 30 minutes and continued for up to 3 hours. In other cases, units characterized 
in normal tissue were treated with saline. The injection of saline and subsequent retests 
were identical to those used with carrageenan. In other cases, response properties of 
separate populations of TMJ afferents were examined only in normal or pre-inflamed 



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14 









DEMONSTRATION OF SENSITIZATION 
SHIFT OF STIMULUS-RESPONSE CODING FUNCTION 

- Ln >riterval (msec) 



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Ln Force (Newtoos) 
— ▼— Finctioo A — •— FLnctioo B 



Figure 2-3. Demonstration of sensitization as a shift of stimulus-response 

functions. Shifts of significant stimulus-response functions to graphic 
zones of enhanced reactivity (below and to the left) suggests 
sensitization. For downward shifts, each point on line B represents a 
higher rate of discharge (shorter interval) at an equivalent force. For 
leftward shifts, reactivity appears at forces which previously were 
ineffective. 



■."■.., ■ ^- - . , f . ■- 

tissue. In this instance, inflammation was induced at least 6 hours before recording began. 
Carrageenan (2%, 200 |xl) was injected into the lateral and posterior aspects of the TMJ 
capsule as well as the superior joint space. "" ; ' ' -;. 









^, CHAPTERS < 

RESULTS 
Identificarion of TMJ Nociceptors 

Receptive fields for units with VP or HP reactivity were found on the lateral and 
posterior capsule of the TMJ (Figures 3-1 and 3-2). The mean von Frey thresholds for VP 
and HP units were 27 ± 39 g and 15 ± 20 g, respectively. The receptive fields of these 
units were single, small spots (approximately 2-3 mm). In some cases, receptive fields 
could not be identified. It is possible that the receptive fields of these units were located on 
the medial capsule, posterior attachment tissues or peripheral portions of the articular disc. 
Alternatively, it is possible that units without identified receptive fields were not of TMJ 
origin but, instead, of muscular origin (lateral pterygoid or temporalis muscles). 
Conduction velocities were determined to be in the group III and IV fiber range (0.4 to 8.5 
m/s). Due to die inaccessibility of many of the receptive fields, conduction velocities could 
only be obtained for 30% of the units (19 of 63 units). 

The response characteristics of TMJ afferents were examined. Mechanical 
reactivity to jaw movement was determined using both dynamically and statically applied 
forces. In order to distinguish between joint afferents acting as proprioceptors from those 
acting as nociceptors,we searched for afferents with a preference for intense stimuli. It was 
predicted that TMJ nociceptors would respond in the noxious range of mandibular motion, 
where the noxious range of motion was defined as that passive mandibular motion where 
the mandible encounters considerable resistance imposed by constraints of soft tissue. 



16 



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Figure 3-1. Receptive field (RF) distribution in the lateral and posterior capsule of the 
TMJ for normal tissue. A) Distribution of RFs in the lateral capsule. B) 
Distribution of RFs in the posterior capsule. RFs (n=36) of afferents in 
A) and B) responded to either vertical plane (.) or horizontal plane (A) 
movement of the mandible. POST, posterior; ANT, Anterior, MED, 
medial; LAT, lateral. 



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POST 




ANT 



B 



MED 




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Figure 3-2. 


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Receptive field (RF) distribution in the lateral and posterior capsule of the 
TMJ for previously inflamed tissue (•), acutely inflamed tissue (a) and 
saline control tissue (+). A) Lateral capsule. B) Posterior capsule. 
. POST, posterior, ANT, anterior, MED, Medial; LAT, lateral. 




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21 



Therefore, relationships between applied force and jaw movement were examined to 
determine the noxious range and compare it with afferent discharge properties. 

Due to physical constraints of tiie preparation, force-movement relationships could 
only be examined for VP units. Characterization of force-movement relationships in the 
vertical plane revealed a biphasic relationship between applied force and mandibular 
movement (Figure 3-3). Linear force-movement relationships gave way to exponential 
force-movement relationships when the mandible reached an extreme of opening. It is 
likely that this exponential phase corresponds to the noxious range. Force-movement 
curves of VP units (n = 10) were best described by power functions (Table 3-1). Power 
functions were the best fit in 10 of 10 cases (R^ = 0.92 + 0.06). The functional range of 
VP units may be graphically assessed by observing activation thresholds plotted on force- 
movement curves. As can be seen in Figure 3-3, nearly all afferents began to respond in 
the transition zone between the linear and exponential phases of the curves. This can be 
examined statistically by examining the functions fit below the point of activation. For the 
10 cases in which power functions were fit, activation threshold occurred during portions 
of the curves which were exponentially accelerating (6/10 cases, R^ = 0.86 + 0.17). In 4 
cases, activation thresholds occurred in portions of the curve in which force was increasing 
linearly (R^ = 0.88 + 0. 19). The activation thesholds of these 4 units occurred at forces 
approaching the power phase of the curve. The observed preference for high forces (mean 
activation threshold for force = 20.6 + 1 1.0 N; mean frequency asymptote = 49.6 ± 20.7 
N) at extremes of the range of motion (mean activation threshold at 1 3.7° + 5.4°; mean 
frequency asymptote = 20.4 + 5.9°) suggested that these TMJ afferents were nociceptors. 

Characterization of TMJ Nociceptors in Normal Tissue 

Units were classified according to their preferred movement plane. Preferred 
movement was defined as that plane of motion in which mandibular excursion evokes the 



' ■:£■ • 



■> ■■ i. 



-; V^ 



Figure 3-3. Relationships between applied force and venical plane movements of the 
mandible. Ten biphasic curves indicated that low forces were sufficient to 
open the jaw through most of its range of motion. High forces produce 
minimal degrees of opening where the joint encounters considerable 
resistance from soft tissue. In each case, the TMJ nociceptor begins to 
respond at the point indicated by the arrow. 



23 



TMJ FORCE/MOVEMENT RELATIONSHIPS: VERTICAL PLANE 



MOVEMENT (dagreea) 




MOVEMENT (dagreasi 








..Mttlf^ 


^fft^;;^* 


J^ 


/ 


f 






N042090H 



100 120 140 



10 20 30 40 SO 00 70 



FORCE (Nairtana) 

■*- TEST -•- TEST -•- TEST -■- TEST 
12 3 4 



FORCE (Nawlonaj 

■»- TEST-*- TEST-*- TEST-*- TEST-*- TEST 
1 2 3 4 S 



B 



MOVEMENT 


dagrefls) 




■ 




•»i****^^*~^ 


i 


V^ 


f 




i 


N111490D 



MOVEMENT (()eof»«8) 



1* t 


•M'"***-*^^'"^ 


/>^' 


^* 




1 


N111490D 



15 30 45 »0 75 BO 105 120 135 150 



15 30 45 00 75 90 105 120 135 150 



FORCE (NawtOfia) 

■*- TEST-*- TEST-*- TEST-"- TEST-*- TEST 
12 3 4 5 



FORCE (Nawtona) 

"*- TEST-*- TEST-*- TEST-"- TEST-*- TEST 
I 2 3 4 S 



MOVEMENT (Degrees) 




FORCE (Nawtona) 

■»- TEST-*- TEST-*- TEST-"- TEST-*- TEST 
1 2 3 4 S 



MOVEMENT (deareesl 



« . ♦' #««» "* ' 



^^ 



^ 



t 



5 10 IS 20 25 30 35 40 4S 



■*- TEST 
1 



FORCE (Nawtona) 

-•- TEST 
2 



-*- TEST 

3 



■I -i i 



24 



TMJ FORCE/MOVEMENT RELATIONSHIPS: VERTICAL PLANE 



MOVEMENT (ilear«««) 





_^*— .-— — • 




_L^ 


,^^ 


^ 






j 


^ 


if 


f 


' 


I ..... . 




1 . . . 


ososgic 





MOVEMENT (d»Qr««») 



10 20 30 40 SO 60 70 80 
FORCE (Nawtons) 

■*- TEST -•- TEST -♦- TEST -■- TEST 

12 3 4 




■*- TEST 
1 



FORCE (Nawtons) 

-•- TEST 

2 



■♦- TEST 

3 



H 



MOVEMENT (dagfees) 




^ 



10 20 30 40 50 60 70 



FORCE (Nawtona) 



I- TEST 
1 



TEST 
2 



■♦- TEST 

3 



TEST 

4 



MOVEMENT Ideofees) 




^ 



17 



r 



10 20 



TEST 
1 



FORCE (Nawlona) 



TEST 
2 



Figure 3.3. (cont'd) 





' 


25 

Table 3-1 








:■ 


Force/Movement Relationships in the Vertical Plane 










RLE 


FUNCTION 


FULL RANGE 


LOW RANGE 


2 
R 


P 




042090H 


POW 


Lnl = 0.69 LnF + 4.8 




0.93 


0.0001 




042090H 


LIN 


I = 0.15F+ 1.8 




0.90 


0.0001 






042090H 


POW 




Lnl = 0.8 LnF + 0.89 


0.96 


0.0001 






042090H 


LIN 




I = 0.2F + 0.87 


0.95 


0.0001 






110990E 


POW 


Lnl = 0.8 LnF + 2.1 




0.97 


0.0001 






110990E 


LIN 


I = 0.6 F + 2.3 




0.96 


0.0001 






110990E 


POW 




Lnl= 1.1 LnF+ 0.15 


0.92 


0.0001 






110990E 


LIN 




1 = 1.0 + 0.19 


0.97 


0.0001 






111490D1 


POW 


Lnl = 0.4 LnF + I.l 




0.91 


0.0001 






111490D1 


LIN 


I = 0.1F + 8.5 




0.87 


0.0001 






111490D1 


POW 




Lnl= 1.7 LnF + 2.2 


0.92 


0.0001 






111490D1 


LIN 




I=1.0F + 4.2 


0.86 


0.0001 






111490D2 


POW 


Lnl= 1.3 LnF + 1.2 




0.91 


0.0001 






111490D2 


LIN 


I = 0.7F+ 0.22 




0.87 


0.0001 






111490D2 


POW 




Lnl = 2.3 LnF + 3.5 


0.94 


0.0001 






111490D2 


LIN 




1= 1.4F + 7.4 


0.97 


0.0001 






022791 A 


POW 


Lnl = 0.3 LnF + 2..2 




0.93 


0.0001 






022791 A 


LIN 


I = 0.77F+ 11.0 




0.79 


0.0001 






022791 A 


POW 




Lnl = 0.15 LnF +2.0 


0.80 


0.04 






022791 A 


LIN 




1= 1.8F + 5.9 


0.97 


0.0001 






03289 IX 


POW 


Lnl = 0.37 LnF +1.1 




0.99 


0.0001 






03289 IX 


LIN 


I = 0.23F + 3.7 




0.88 


0.0001 






03289 IX 


POW 




Lnl = 0.4 LnF + 0.01 


0.98 


0.0001 






03289 IX 


LIN 




I = 0.55F + 2.3 


0.88 


0.0001 






08059 IC 


POW 


Lnl = 0.34 LnF +1.9 




0.87 


0.0001 






08059 IC 


LIN 


I = 0.28F+ 12.0 




0.77 


0.0001 






080591C 


POW 




Lnl = 0.46 LnF + 1.8 


0.57 


0.0003 






08059 IC 


LIN 




1= 1.5 F + 5.3 


0.61 


0.0001 






091691A 


POW 


Lnl = 0.54 LnF + 1.3 




0.87 


0.0001 






091691A 


LIN 


I = 0.42F + 9.0 




0.83 


0.0001 






091691A 


POW 




Lnl = 0.64 LnF +1.2 


0.52 


0.01 






091691A 


LIN 




I = 2.3F+ 1.3 


0.37 


0.04 






09279 IK 


POW 


Lnl = 0.48 LnF + 1.4 




0.96 


0.0001 






09279 IK 


LIN 


I = 0.37 F + 8.6 




0.88 


0.0001 






09279 IK 


POW 




Lnl = 0.59 LnF + 1.3 


0.90 


0.0001 






09279 IK 


LIN 




I = .97F + 4.1 


0.88 


0.0001 






101891F 


POW 


Lnl = 0.5 LnF + 1.3 




0.83 


0.0001 






101891F 


LIN 


I = 0.29F+ 11.0 




0.73 


0.0001 






101891F 


POW 




Lnl = 0.74 LnF + 1.0 


0.86 


0.0001 






101891F 


LIN 




I = 0.9 F + 5.6 


0.64 


0.0001 




Note: POW 


, power, LIN 


, linear. 












-.. ■--..^^ -'■^■■cJ..'' ^ ^-"^ 


















;■ _ -■ i 










■ , i -. . . 


" V;:; <: ■■ ■.^.., . , J 









26 



strongest response from an afferent. Thirty-six afferents with receptive fields in the TMJ 
capsule were activated by either vertical plane (VP or opening) or horizontal plane (HP or 
lateral displacement) motion. Eighteen afferents responded preferentially to movement in 
the vertical plane and 18 responded best to movement in the horizontal plane. A few units 
were activated by right lateral displacement (n = 5) or protrusive (n = 2) movement but 
most TMJ afferents responded preferentially to either opening (VP) or left lateral 
displacement (HP). ^ f . >„»>><--*-• « 

Once preferred movement was determined, tests of dynamic and static reactivity 
were conducted. Relationships between force, position or movement and response interval 
were quantified. The responses of TMJ nociceptors were quantified by regressions fit 
between instantaneous dynamic force, force velocity, movement, static force or position 
and instantaneous interspike interval. 

As it was not clear which function would best describe TMJ afferents, linear, 
power, logarithmic and exponential models were explored. By comparison of the relative 
proportions of variance accounted for by each model, it was determined that power 
functions accounted for the greatest percentage of variance (mean R^ - 0.46 + 0.26; n = 71 
cases). Power functions were best fits compared to other functions for both dynamic 
(26/59 cases) and static tests (10/12 cases). Power functions were second best fits in 20 
out of 59 cases for dynamic tests and 1 out of 12 cases for static tests. Linear functions 
were superior in 7 cases, logarithmic in 12 cases and exponential in 16 cases. Since power 
functions were the best or second best fit in 46 of 71 cases (mean R^ = 0.45 ± .30), power 
functions were used to represent the data in normal tissue. In inflamed tissue (both PI and 
AI), power functions accounted for the greatest percentage of variance in 101 of 146 cases 
(mean R2 = 0.50 ±0.21). 

TMJ nociceptors could be found which transduced (or coded) all aspects of force, 
movement or position, and many transduced more than one variable. "Code" indicates that 



..:4 /■ 27 



a unit's reactivity was proportional to force or some other stimulus variable and that the 
relationship could be described by a significant power function. 

The great majority of TMJ nociceptors (n = 24) coded dynamic aspects of force 
applied to the mandible, and relatively few coded for static aspects of these stimuli. 
Twenty-three of 36 units that responded to either VP or HP jaw movement coded for 
dynamic force (mean activation threshold = 20.1 ± 17.5 N) and 15 of 36 units coded for 
force velocity (mean activation threshold = 15.5 ± 20.5 N/s; Table 3-2). In contrast, only 
8 of 36 units coded for static force (mean activation threshold 17.8 ± 18.3 N), while 5 of 

35 units coded jaw movement (mean activation thresholds of 1 1.0° ± 4.0°, and only 1 of 

36 units coded for jaw position. In some cases, unit reactivity could be described by more 
than one function. Twelve of 23 units that could be fit to dynamic force were also 
significantly fit to force velocity. Six of these 12 units were significantly fit to force 
velocity, and 6 of these 12 units were signficantly fit to static force as well. Ten of 36 units 
could not be fit to any function. Fourteen additional units had jaw movement reactivity but 
no receptive field could be found. 

Mean functions were generated from individually fitted functions by pooling 
slopes, intercepts and boundary values. Functions presented in Figure 3-4 represent the 
principle transducing properties of TMJ afferents: dynamic force and force velocity. 

Properties of TMJ Nociceptors in Inflamed Tissue 

The response properties of afferents were examined in capsular tissue that was 
previously inflamed (PI) by carrageenan. In these experiments, TMJ tissues were exposed 
to carrageenan for at least 6 hours prior to testing. In other experiments, afferents were 
tested in normal tissue and then tested again after an acute injection of carrageenan or 
saline. Afferent reactivity was examined for up to 3 hours subsequent to exposure to 
carrageenan. 



28 



TABLE 3-2 



TMJ NOCICEPTOR REACTIVITY IN NORMAL TISSUE 



Test Conditions 


with RF (n=36) 


without RF(n= 14) 


code (n=25) 


no code (n=10) 


code (n=9) 


no code (n=5) 


Dynamic Force 


23 


12 


6 


6 


Force Velocity 


15 


19 


4 


8 


Movement 


5 


10 


2 


3 


Static Force 


8 


23 


1 


4 


Static Position 


1 


14 





4 


Conduction 
Velocity 


0.4 to 7.5 

m/sec 

(n = 6) 


0.5 to 1.5 

m/sec 

(n = 3) 


• 


• 


Post-test 
Spontaneous 

Activity 


3 












Note: Receptive fields (RF) in the TMJ capsule were identified for 36 units. Twenty-five 
units with RFs coded for one or more of the stimuli. Most units (n = 23) with an 
RF on the TMJ capsule coded for dynamic force. Fourteen additional units had 
either VP or HP reactivity but an RF could not be found. "Code" indicates that a 
unit's reactivity could be described by a significant power function. Of the 36 
afferents with RFs in the TMJ capsule, 3 units demonstrated spontaneous 
activity after dynamic or static testing. Five units with RF's in the TMJ capsule 
responded preferentially to right lateral displacement. Most of these units ( 3 of 
5 cases) coded dynamic force. Appendix G contains descriptive statistics for 
these units. 



r 


, ..:^' 5.1:': 




us dynamic 
ment in the 
ope = -1.3 ± 
n opening of 
iredto 
equency. B) 
86.0 N/s; 
; range = 9.7 
;an slope = - 




n instantaneo 
idibular move 
orce (mean si 
ated at a mea 
Dvement requ 
St response fr 
.5 to 157.0 ± 
s = -0.9 ±0.7 
; velocity (me 




■•■':. 




.-.,:: 


the relationship betwee 
ents responding to man 
> transduced dynamic f 
These units were activ 
the smallest force or mi 
hat produced the highe 
0.2; range =17.5 ±19 
amic force (mean slopi 
units transduced force 
7 ±0.14). 


■<■: 


s best described 
interval for affer 
;nof ISVPunit; 
= 0.46 ±0.21). 
was defined as i 
e of movement t 
n slope = -0.6 ± 
transduced dyn 
Seven of 18 HP 
; mean R2 = 0.2 














tissue. Power fun 
instantaneous resp 
ontal plane (HP). 
8.5 ± 22.0 N; mea 
ivity of each nocic 
ise frequency to th( 
ced force velocity 
Thineenof 18 HP 
1 R2 = 0.39 ± 0.24; 
6.9 to 166.0 ±92. 




" ^•■" 


lormal 
' with 
horiz 
5 to 4 
of act 
espon 
ansdui 
). C) 
mean 
.9±1 




Dynamic reactivity in n 
force and force velocity 
vertical plane (VP) and 
0.2; range = 17.0 ±33. 
11.2 ±4.4°. The range 
produce the minimum r 
Eightof 18 VP units tri 
mean R2 = 0.30 ±0.1 8 
±7.3 to 37.0 ± 22.8 N; 
0.39 ± 0.24; range = 7, 


>-•■- 








- : ^ 




tn ^: i. 




■'.-,«» 




ta 


't* 


■f /' ■ 3 
'■■ : Ml 


v< 






fa. 


.■^ - ■ - ■■ ■ 


-"-•*■ .» - S'-', f: -y ■ _ ■:■ 


'.'*': 




■ -- i 





30 



z 
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31 



Experiment I: Properties of Units in the 
Previously Inflamed TMJ 



In the PI condition, transduction of the dynamic aspects of stimulus force was best 
described by power functions. Power functions were the best fit compared to other 
functions (7 of 13 cases; R^ = 0.33 ± 0.25) and were best or second best fit in 9 of 13 
cases. Therefore, exposure to carrageenan did not modify the nature of functions which 
described afferent activity. Individually fitted power functions generated during dynamic 
and static response testing in inflamed tissue are illustrated in Figure 3-5. 

Comparison of units in normal and inflamed tissue (see Figure 3-6) suggested 
improved reactivity for units that responded preferentially to movement in the vertical 
plane. Increased reactivity to dynamic stimuli was particularly prominent. In normal 
tissue, 1 1 of 1 8 units with RFs on the TMJ capsule coded for dynamic force or velocity; 
while proportionally more units (5/5) transduced dynamic force or velocity in the PI 
condition. Mean functions for dynamic force in inflamed and noninflamed conditions were 
calculated by averaging slopes and intercepts of individual functions (Lnl = -1.3LnF + 7.3, 
(n = 25); Lnl = - 1.1 LnF + 5.4, (n = 6)] for inflamed and noninflamed, respectively). The 
mean functions for all VP and HP units fitted during dynamic testing in normal and 
inflamed tissue suggested improvement of dynamic reactivity (Figure 3-6). The shifts of 
the mean function for units in PI condition to a graphic position below the mean function 
for normal tissue was suggestive of sensitization to dynamic forces. 

Mean functions were also calculated for afferents transducing force velocity. A 
shift of the mean function of PI units that coded for force velocity [Lnl = -0.7 LnF + 3.5, 
(n = 6)] was also observed in comparison to the mean functions in normal tissue [Lnl = - 
0.38 LnF -i- 4.7, (n = 16)]. These functions are illustrated in Figure 3-6. A shift of the 
mean function for afferents in inflamed tissue below and to the left of the mean function for 
normal tissue also suggested sensitization to velocity of applied forces. 



"^ ^ . ; ^ i 









Figure 3-5. Dynamic reactivity in previously inflamed tissue. Power functions best 
described the relationship between instantaneous dynamic force and force 
velocity with instantaneous response interval in the vertical or horizontal 
plane. A) Six of 7 units transduced dynamic force (mean slope = -1.1 + 
0.5; range = 7.6 ± 10.2 to 33.3 ± 32.1 N; mean R2 = 0.24 ± 0.16). B) 
Six of 7 units transduced force velocity (mean slope = -0.7 ± 0.8; range = 
4.8 ± 4.5 to 40.2 ± 22.2 N/s; mean r2 = 0.33 ± 0.28). 



33 



REACTIVITY IN PREVIOUSLY INFLAMED TISSUE: 
DYNAMIC FORCE 

_ Ln Interval (msec) 




^ 



/^ I i i I i 1 i I 1 1 1 I 1 I I I ■ ' ' I I I I I i_ 

-1.5 0.0 1.5 3.0 4.5 6.0 

Ln FORCE (Newtons) 
-▼- T7 -♦- El -■- J1 -•- E3 -^- T1 - + - 02 



REACTIVITY IN PREVIOUSLY INFLAMED TISSUE; 
FORCE VELOCITY 



Ln Interval 


(msec) 












O. 


■ \ 






A 




-A 




*^=i^ 


^ 


V 




■--■1^*^^==* 






=•+ 


■ 


\ 






'^~^~^ 




■^•1. 


' 1 < 1 1 I 


\ 

. , . 1 


V 


1 ■ ' ■ 1 1 1 




— 1 1- 





-1 



o 



1 



Ln Velocity (Newtons/sec) 
- + - B2 -A- T7 -O- El - + - J1 -A- E3 -•- T1 



4. ' ■ 



_" ■' \ -..■*. 



, ^ ,V- :»^ . - 



J" y i_ ''q t 



Figure 3-6. Averaged dynamic response functions of nociceptors fitted in normal and 
previously inflamed tissue (PI). A) Mean function for dynamic force 
fitted in PI tissue (mean interval = 29.9 ± 7.9 msec) falls below the mean 
dynamic force function fitted in normal tissue (mean interval = 44.7 ± 
16.5 msec) suggesting sensitization. B) Mean function for force velocity 
in PI tissue (mean interval = 22.2 + 3.3 msec; mean activation threshold = 
17.3 + 18.9 N/s) falls below and to the left of mean force velocity 
function fitted in normal tissue (mean interval = 7.4 + 4.8 msec; mean 
activation threshold = 4.8 + 4.5 N/s) suggesting enhanced reactivity 
(sensitization) 



^ 35 






*--» 



CHANGES IN REACTIVITY TO DYNAMIC FORCE 
FOLLOWING CARRAGEENAN INFLAMMATION 



Ln Interval (msec) 






-T- N (n=25) 



2 3 4 

Ln Force (Newtons) 

-•-INF (n=6) 



B CHANGES IN REACTIVITY TO FORCE VELOCITY 
FOLLOWING CARRAGEENAN INFLAMMATION 



Ln Interval (msec) 








■ 


■ . ■ 


T^_^^__^ 


•^..^^^^ 






~~-T 


^^^^ 


'■ — 1 1 1 1 1 1 1 1 1 l_ 


J ...1. 1 1 1 


1 1 1 1 1 





O 1 2 ,34 5 

Ln Velocity (Newtons/sec) 
-▼- N (n=16) -•- INF (n=6) 



■} ' ' t -'A h 



i*» 



r.J 



J ■',, 



36 



Statistical comparisons between function characteristics in normal and inflamed 
tissues confirmed that dynamic reactivity improved in inflamed tissues (See Table 3-3). 
This was manifested as changes in activation threshold, frequency asymptotes and function 
intercepts. The mean activation threshold (8.3 ± 13.2 N) for units in inflamed tissue (n = 
4) that responded best to jaw opening and transduced dynamic force was significantly 
lowered relative to the mean activation threshold (24.1 + 11.2 N) for VP units (n = 10) in 
normal tissue (F = 5.36, df = 13, p < 0.04). For those same units, the mean intercept in 
inflamed tissue (5.0 ± 3.0) was significantly decreased relative to the mean intercept in 
normal tissue (9.0 ±3.1). Similar changes were observed for afferents that transduced 
force velocity. The mean frequency asymptote (37.5 ± 23.6 N/s) for these units was 
significantly less than the mean frequency asymptote (148.0 ± 79.6 N/s) for units (n = 8), 
in normal tissue (F = 8.89, df = 12, p < 0.01). The mean force-frequency asymptote (40.2 
± 22.2 N/s) for PI units (n = 6) that coded for force velocity in both VP and HP jaw 
movements were significantly less than the mean force-frequency asymptote (156.5 ± 83.1 
N/s) for VP and HP units (n = 15) in normal tissue (F = 9.57, df = 21, p < 0.01). 

The changes we have observed in dynamic reactivity of TMJ nociceptors are 
suggestive of sensitization. However, experiments of this type (PI tissue) are subject to 
sampling errors. The best form of evidence for nociceptor sensitization comes from 
observations of single affferents making transitions from the normal to the sensitized state, 
following acute injections of pro-inflammatory substances. 



Experiment II: Properties of Units in the 
Acutely Inflamed TMJ 



The findings of enhanced dynamic reactivity observed in populations of afferents 
sampled from normal and subacutely inflamed TMJ tissues were complemented by 
observations made on units in which testing was performed before and after carrageenan- 



37 



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39 

,-* . J* -^ r 

induced inflammation (acutely inflamed or AT). Outcomes of experiments using PI 
methods suggested that individually characterized afferents would manifiest improved 
dynamic reactivity. 

Observations of quantitative shifts in force interval functions were confirmed, and 
additional qualitative changes were observed. Eleven units were characterized in normal 
tissue and then retested 1-3 h after exposure to carrageenan. Four units responded 
preferentially to VP jaw movement and 7 responded best to HP movement. For 9 units that 
transduced stimulus intensity in both normal and inflamed tissue, 6 demonstrated enhanced 
reactivity for dynamic force (Figure 3-7). Four of these 6 units had post-inflammatory 
functions that shifted below the pre-inflammatory function. One of these also showed 
leftward shift. Three of 6 units that demonstrated enhanced dynamic force reactivity 
showed a leftward function shift relative to pre-inflammatory functions but failed to shift 
below the control case. Mean function characteristics for these nociceptors are presented in 
Table 3-3. ■ 

Experiments were performed to determine whether changes in AI reactivity 
occurred as a result of carrageenan or other causes, such as repeated stimulation. In these 
control experiments, saline (1(X) [i\) was injected into the area of the RF and into the TMJ 
capsule. Reactivity was examined in 8 units after exposure to saline. Five of 8 units 
transduced dynamic force in both the pre- and post-saline conditions. While quantitative 
changes in reactivity were small following saline injections, there was some indication that 
repeated testing could produce qualitative changes in reactivity similar to those observed 
following carrageenan injection (See Figure 3-8). 

Following saline injection, mean activation threshold was reduced from 14.1 + 
15.0 N in pre-saline condition to 1 1.5 ± 7.5 N . These changes were relatively small 
compared to changes observed following carrageenan (1 1.2 + 9.9 to 5.1 ± 3.7 N). 
Statistical comparisons indicated that the mean changes in activation threshold was 
significantly less in saline than carrageenan treated cases (T = -2.2; DF = 15; p = 0.04)). 






t ♦ 



Figure 3-7. Demonstration of sensitization (enhanced reactivity). Six of 1 1 units 
were characterized in normal tissue and then tested again after acutely 
inflamed (AI) with carrageenan. Power functions generated from 
retesting in acutely inflamed tissue were positioned below and/or to the 
left of power functions fitted on normal tissue. N, normal, Min, 
inflamed; HR, inflamed. 



~;r ■ 



41 



REACTIVITY IN VERTICAL PLANE: NORMAL TO INFLAMED 
DYNAMIC FORCE: UNIT #1 



-♦- 1 ►*! -•- 3 h« 



REACTIVITY IN HORIZONTAL PLANE: NORMAL TO INFLAMED 
DYNAMIC FORCE: UNIT #2 

5 io_t3*saLb»e^ 




3 3 4 

Ln Fore* ♦lawto m ) 
-♦- 1 l-B 



B 



REACTIVITY IN VERTICAL PLANE: NORMAL TO INFLAMED 
DYNAMIC FORCE: UNIT #3 



■n tnlfvl ttv6%ci 



REACTIVITY IN HORIZONTAL PLANE: NORMAL TO INFLAMED 
DYNAMIC FORCE: UNIT #5 

g Ln IntTVI tms«cf 



\ 



Ln Pore* tf'Jr-vlcn*} 

-♦- 1 »-« 



Ln Fore* t4awtona> 

-♦- as I 



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DYNAMIC FORCE: UNIT #4 

- Ln M<rv»l Unt»c) 



Ln Farc« t^iawtora) 
-♦- 90 Mn -■- 2 f« 



REACTIVITY IN HORIZONTAL PLANE: NORMAL TO INFLAMED 
DYNAMIC FORCE: UNIT #6 



Ln lnt«rv»l frnsAc) 


















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^* 








\ 






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:- ■: « 



Figure 3-8. Reactivity of nociceptors exposed to saline. Five units transduced 

dynamic force in both the pre- and post-saline conditions. A) and B) 
demonstrate quantative changes in dynamic force reactivity. C), D) and 
E) show no enhanced reactivity. 



f 



43 



REACTIVITY IN HORIZONTAL PLANE: SALINE CONTROL 
DYNAMIC FORCE: LEFT LATERAL UNIT #3 



■n >lt»v»J <pn—c) 



2 3 

-•- Sim 



B 



REACTIVITY IN HORIZONTAL PLANE: SALINE CONTROL 
DYNAMIC FORCE: LEFT LATERAL UNIT #6 




Ln f=crc« M*wton«t 

-♦- Sim 



REACTIVITY IN HORIZONTAL PLANE: SALINE CONROL 
DYNAMIC FORCE: LEFT LATERAL UNIT #2 



Ln W«rv« Irmtd 










,«--^ 




^^■^^^ 






™„ 



D 



REACTIVITY IN HORIZONTAL PLANE: SALINE CONTROL 
DYNAMIC FORCE: LEFT LATERAL UNIT #7 



Ln Foro* rJ»wton«J 
-♦- SIHB - 



Ln Fcrc* ^*•wto^■J 
-♦- SlKR - 



REACTIVITY IN HORIZONTAL PLANE: SALINE CONTROL 
DYNAMIC FORCE: RIGHT LATERAL UNIT #1 

e 

5 



J\ W«v»l (mMd 


\ 


*^^^N-\ 




^' 






— 






44 



Therefore while shifts in activation threshold could occur following repeated testing, the 
changes that followed carrageenan injection were significantly greater. 

In experiment I, it was determined that most TMJ nociceptors transduced dynamic 
force and velocity, but few transduced either static force, movement or position. 
Following acute exposure to carrageenan, qualitative changes in coding capacities were 
noted; that is, afferents coded for stimulus features not previously transduced. 

Qualitative improvements were observed for most units for either dynamically or 
statically applied stimuli. Eight of 1 1 nociceptors acquired either dynamic or static coding 
ability (Table 3-4). Four of 4 units that preferred VP jaw movement and transduced 
dynamic force in normal tissue acquired the ability to transduce force velocity (n = 2), static 
force (n = 1) or jaw position (n = 1) in inflamed tissue. Two of 5 AI units that preferred 
HP movement and transduced dynamic force in normal tissue also acquired the ability to 
transduce static force. Acquired coding also appeared in nociceptors that were without 
transducing capacity in normal tissue. Two of 7 AI units that preferred HP movement 
acquired the capacity to transduce both dynamic and static force. Other changes appeared 
as de novo reactivity. Three of 7 units that had only HP jaw movement initially acquired 
similar reactivity for VP movement (dynamic force). Six units demonstrated spontaneous 
activity after stimulus testing. ",.„/; ' . '' 

The finding that a large proportion (8/11) of nociceptors acquired coding ability 
after exposure of carrageenan suggested a qualitative form of sensitization. The nature of 
these qualitative changes can be best appreciated by comparing scatter plots representing 
comparisons between pre-inflamed and post-inflamed reactivity. Two types of trends (shift 
and rotation) were observed. Shift indicates a movement of a scatter of points into graphic 
zones of greater sensitivity. Rotation indicates the development of a significant slope 
associated with the scatter field of points. Of the 9 of 1 1 nociceptors that acquired coding 
ability, all 9 showed shifts and/or rotation. Figure 3-9 illustrates significant functions of 
units that demonstrated shifts and units that demonstrated rotation of scatter point fields. 



45 



M 



Table 3-4. 



EFFECT OF CARRAGEENAN ON TRANSDUCING CAPACITY 

Qualitative improvements in reactivity for nociceptors that were 
characterized in nonnal tissue and then tested again subsequent to 
carrageenan injection. Eight of 1 1 nociceptors acquired either dynamic or 
static coding ability. Coding ability was also acquired for nociceptors (n = 
2) that had no transducing capacity in nomial tissue. Three units that 
responded to horizontal plane movement acquired vertical plane reactivity in 
acutely inflamed tissue. Six units demonstrated spontaneous activity after 
stimulus testing in acutely inflamed tissue. 



UNIT 


PU\NE 


PRE-INFLAMED 


POST-INFLAMED 


CODING 
SHIFT 


OTTER 
MOVEMENT 


POST-TEST 

SPONTAN. 

ACTIVITY 


1 


VP 


DYNAMIC FORCE 

MOVEMENT 
STATIC FORCE 
POSITION 


DYNAMIC FORCE 
FORCE VELOCITV 
MOVEMENT 
STATIC FORCE 
POSITION 


YES 


• 


YES 


2 


VP 


DYNAMIC FORCE 


DYNAMIC FORCE 
STATIC FORCE 


YES 


• 


YES 


3 


VP 


DYNAMIC FORCE 
STATIC FORCE 


DYNAMIC FORCE 
FORCE VELOCITY 
STATIC FORCE 


YES 


• 


Norc 


4 


VP 


DYNAMIC FORCE 
FORCE VELOCITY 
MOVEMENT 


DYNAMIC FORCE 

MOVEMENT 
POSITION 


YES 


• 


NDNE 



Note: VP, vertical plane 



46 



Table 3-4 (cont'd). 



UNIT 


PLANE 


PRE-INFLAMED 


POST- INFLAMED 


CODING 
SHIFT 


OTHER 
MOVEMENT 


POST-TEST 

SPONTAN. 

ACTIVITY 


5 


HP 


• 


DYNAMIC FORCE 
FORCE VELOCITY 
STATIC FORCE 


YES 
YES 
YES 


• 


YES 


6 


HP 


DYNAMIC FORCE 
FORCE VELOCITY 


DYNAMIC FORCE 
FORCE VELOCITY 
STATIC FORCE 


YES 


• 


YES 


7 


HP 


DYNAMIC FORCE 
FORCE VELOCITY 


DYNAMIC FORCE 
FORCE VELOCITY 
STATIC FORCE 


YES 


OPEN: CODE 
OPEN: CODE 
OPEN: NON-CODE 


Nort 


8 


HP 


DYNAMIC FORCE 
FORCC VELOCITY 
STATIC FORCE 


DYNAMIC FORCE 
FORCE VELOCITY 
STATIC FORCE 


• 


• 


YES 


9 


HP 


DYNAMIC FORCE 


DYNAMIC FORCE 


• 


OPEN: CODE 


YES 


10 


HP 


DYNAMIC FORCE 
STATIC FORCE 


DYNAMIC FORCE 
STATIC FORCE 


• 


• 


Nor^ 


11 


HP 


• 


DYNAMIC FORCE 
FORCE VELOCITY 
STATIC FORCE 


YES 
YES 
YES 


OPEN: NON-CODE 
OPEN: NON-CODE 
OPEN: NON-CODE 


NDTC 



Note: HP, horizontal plane 



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50 



Of the 9 units exhibiting rotation, 4 also shifted. It was possible that shift was a more 
mature form of sensitization that followed rotation. In units which were examined over 
several hours, 2 of 2 units that exhibited rotations subsequently manifested shifts of their 
scatter plot field (See Figure 3-9). ., 

Control tests indicted that qualitative changes could also be observed after saline 
injection. In 1 of 8 cases, a qualitative improvement was observed in dynamic coding 
capacity (Table 3-5). Thus, improved dynamic reactivity is possible as the result of saline 
injection. However, the tendency towards acquired coding appeared to be greater for 
carrageenan-induced inflammation (8 of 11 cases). 

In summary, experiments were performed to characterize the response properties of 
presumed nociceptors in normal and inflamed capsular tissue of the TMJ. Most TMJ 
afferents preferred either movement in the horizontal or vertical plane. Their reactivity 
functions were best described by power functions fit between dynamic force, force velocity 
and response interval. In normal tissue, TMJ afferents had properties of nociceptors, in 
that the activation threshold was at the extreme range of jaw movement, either in the 
exponential portion or in the transition zone between the linear and exponential force- 
movement curves that described jaw movement. It was predicted that TMJ nociceptors 
would sensitize following exposure to carrageenan. To test this, populations of afferents 
were sampled in previouslyly inflamed tissue and their responses compared to those of 
afferent populations in normal tissue. Improved reactivity was observed, especially 
reactivity to dynamic stimuli (dynamic force and force velocity). To avoid sampling errors 
that could have biased these observations, units were characterized in acutely inflamed 
tissue after being characterized in normal tissue. These afferents manifested similar 
quantitative improvements in dynamic reactivity. Additionally, qualitative improvements of 
coding capacity were observed. Acquisition of coding capacity following acute 
inflammation suggested afferent sensitization. 



51 






,;j : " ■ -, • TABLE 3-5 

EFFECT OF SALINE ON TRANSDUCING CAPACITY 



UNIT 


PLANE 


PRE-CODING 


POST-CODING 


CODING 
SHIFT 


OTHER 
MOVEMENT 


POST-TEST 
SPONTAN. 
ACTIVITY 


1 


HP 


DYNAMIC FORCE 
FORCE VELOCTIY 
STATIC FORCE 


DYNAMIC FORCE 
FORCE VELOCITY 
STATIC FORCE 


• 


• 


NONE 


2 


HP 


DYNAMIC FORCE 
STATIC FORCE 


DYNAMIC FORCE 
FORCE VELOCITY 
STATIC FORCE 


YES 


• 


NC»«JE 


3 


HP 


DYNAMIC FORCE 
STATIC FORCE 


DYNAMIC FORCE 
STATIC FORCE 


• 


• 


NCWE 


4 


HP 


DYNAMIC FORCE 
FORCE VELOCn Y 
MOVEMENT 
STATIC FORCE 
POSITION 


• 


• 


• 


NOvfE 


5 


HP 


NONCODING 


NONCODING 


• 


• 


NOvnE 


6 


HP 


DYNAMIC FORCE 


DYNAMIC FORCE 


• 


• 


NC»4E 


7 


HP 


DYNAMIC FORCE 
STATIC FORCE 


DYNAMIC FORCE 
STATIC FORCE 


• 


• 


NOME 


8 


HP 


STATIC FORCE 


STATIC FORCE 


• 


• 


NCT4E 



Note: Changes in reactivity for 8 units after exposure to saline. One of 8 units acquired coding ability 
for force velocity. HP, horizontal plane. 



CHAPTER 4 
DISCUSSION 

Afferents were isolated fix)m the trigeminal ganglion and efforts were made to 
determine whether they had nociceptive properties. Tests included quantification of 
response range, identification of relevant stimulus variables and the tendency to sensitize. 
Afferents that are nociceptors should transduce noxious stimuli (Sherrington, 1947), while 
other joint afferents (proprioceptors) would be expected to be most reactive in the normal 
range of motion, be bidirectionallly sensitive, and exhibit spontaneous activity (Burke et 
al., 1988; Macefield et al., 1990, Dom et al., 1991). 

The relationship between applied force and mandibular movement was examined to 
determine the "noxious range" and compare it with the threshold of afferents. The noxious 
range is likely to correspond to that portion of the force/jaw movement relationship where 
forces increased exponentially with jaw movement. TMJ afferents were activated at or near 
the beginning of the exponential phase and their firing became asymptotic in the exponential 
phase. Thus, a preference for high forces (mean acdvation threshold = 20.6 ± 1 l.ON) at 
extremes of the mandibular range of motion (mean activanon threshold = 13.7 ± 5.4°; mean 
frequency asymptote = 49.6 ± 20.7 N) suggested that these TMJ afferents were 
nociceptors. . 

In contrast, a small group of units (n = 3) had responses to both jaw opening and 
closing. Their properties are distinct from populations of afferents which may be important 
in signalling tissue damage. Their activation thresholds (1.1 + 0.9 N) and range of 
reactivity (1 . 1 ± 0.9 to 10.4 + 4. 1 N) are considerably different from that of nociceptors 
described above, and respond chiefly to innocuous joint movement within the physiological 

52 



53 



range of motion. Afferents with similar properties have been observed in the cat knee joint 
(Dom, et al., 1991). In this study, large diameter afferents (Group II) responded 
exclusively in the normal range of motion, were directionally sensitive, and demonstrated 
no resting activity. Whereas activity in nociceptors is likely to contribute to joint pain, 
these low threshold afferents may contribute to proprioception or sensations of pressure 
(Burke et al., 1988; Macefield et al., 1990; see Appendix B). 

In other laboratories, recordings have been made from group m and IV joint 
afferents innervating the cat knee (Burgess and Clark, 1969; Clark, 1975; Schaible and 
Schmidt, 1983b). Schaible and Schmidt (1983b) divided their joint afferents into 4 
subgroups which were differentiated, in part, by their qualitative response to movement. 
They defined nociceptors as those afferents that responded through, beyond or exclusively 
beyond the normal range of joint motion. These afferents had a steep rise in discharge 
frequency during forceful rotational movements, similar to those described previously 
(Burgess and Clark, 1969; Coggeshall et al., 1983). These observations compare 
favorably with ours, in that intense mechanical stimulation is needed to achieve a maximum 
response. It is difficult to make detailed comparisons between the response properties of 
afferents described by Schaible and Schmidt and others with those in our experiments, as 
no attempt was made by them to quantify the properties of afferents other than local 
pressure thresholds. Our experiments represent the first quantification of nociceptor 
reactivity across a range of suprathreshold stimuli with verification of the relationship 
between movement, response minima and maxima. 

Early experiments created some confusion as to the basic properties of joint 
afferents. Studies that have examined the activity of mechanoreceptors supplying cat joint 
tissues (Burgess and Clark, 1969; Clark and Burgess, 1975; Rossi and Grigg, 1982) 
primarily emphasized proprioception, and addressed the questions as to whether position 
sense is coded by joint or muscle afferent fibers. They determined that joint afferents are 
only responsive at the extremes of the movement range, seemingly ruling out any useful 






y: 



54 



role in proprioception and clouding the functional distinction between free nerve endings 
(nociceptors) and well recognized encapsulated Golgi and Ruffini type end organs which 
are found throughout the capsule (Thilander, 1961; Ishibashi, 1966). Yet, others have 
reported that many afferents respond within the normal range movement (Klineberg et al., 
1971; Lund and Matthews, 1981; Schaible and Schmidt, 1983b; Dom et al., 1991). 
Microneurographic studies appear to have resolved this confusion in favor of the findings 
of Schmidt and company. These studies have examined the behavior of neuronal 
populations that signal joint position and mechanosensibility in humans. Burke et al., 
(1988) recorded responses of joint, muscle and cutaneous mechanoreceptors associated 
with finger joints to position and movement. Whereas most responded at the limits of joint 
rotation, a few afferents responded within the normal range. It is unclear whether the 
former group could code for pain, as pain was never induced by the movements, but the 
latter group appears to be appropriate for proprioceptive function. The relatively small 
population (3 of 16 cases) that provided a proprioceptive code was not dissimilar to our 
own (3 of 36 cases). Microstimulation of similar groups of joint afferents innervating 
finger joints indicated that innocuous sensations of movement or deep pressure were 
evoked (Macefield, et al., 1990). Thus, a proprioceptive role for joint afferents seems to 
be confirmed, although they may represent a small portion of the afferent population. 

Sensitization of TMJ Nociceptors 

Nociceptors in all preparations will sensitize following exposure to extreme heat 
(Burgess and Peri, 1967; Beck et al., 1974; Fitzgerald and Lynn, 1977; Campbell et al., 
1979), mechanical forces (Reeh et al., 1987) or proinflammatory substances (Schaible and 
Schmidt, 1988a; Berberich et al., 1988; Cooper et al., 1991), and these are reflected as 
changes in central reactivity (Neugebauer and Schaible, 1990; see Appendix D). Sensitized 
nociceptors in skin, muscles and joints have enhanced reactivity to thermal, mechanical 



55 






and/or chemical stimuli. In our experiments, where afferents were sampled from 
previously inflamed capsular tissue or where characterized afferents were retested in acutely 
inflamed tissue, a variety of forms of sensitization was found. These changes included a 
significant decrease in mean activation threshold, shifts in stimulus response functions and 
qualitative forms of sensitization. Additional changes were observed for afferents in the PI 
condition (frequency asymptote and intercept) that were not replicated in the AI condition. 

Recent experiments on cat knee joint nociceptors (Schaible and Schmidt, 1988b) 
have also produced evidence of changes in reactivity following carrageenan injection. Over 
half of the units that were classified as nociceptors in normal tissue responded to innocuous 
joint movements in the normal range of motion after inflammation. In effect, such 
enhanced reactivity, from extremes of movement to the normal range of motion indicates a 
decreased activation threshold. In our experiments, decreases in activation threshold were 
observed following carrageenean-induced inflammation. These decreased activation 
thresholds fell within the linear phase of force-movement relationship. 

In our study, qualitative forms of sensitization were also observed. These appeared 
both in carrageenan treated nociceptors (8 of 1 1 cases), and infrequently in saline treated 
controls (1/8). The nature of these qualitative changes can be best appreciated by 
comparing scatter plots representing comparisons between preinflamed and postinflamed 
reactivity. It is important to examine scatter plots because the acquisition of transducing 
ability could have represented a distorted outcome. For example, outliers could have 
rendered functions insignificant where they were otherwise significant. However, 
examination of plots following carrageenan showed new relationships between force and 
response interval and shifts to greater reactivity. 

Two types of trends were observed: rotation and shift. Rotational trends were 
indicated by a change in slopes which suggested increased proportional reactivity. A shift 
to the left represented a decrease in activation threshold that was seen consistently in AI and 
PI conditions for units with extant coding capacity. The shifts that were observed, were 



56 



less likely to be related to the development of qualitative changes than rotation. Rotation 
represents a new functional reactivity in the form of a proportional response to imposed 
forces. The basis of the qualitative changes could be either receptor based metabolic 
alteration secondary to the generation of proinflammatory substances, or could result from 
improved mechanical coupling between the receptor and the applied force. 

Edema is a major component of inflammation that may impact on mechanical 
coupling. Afferent terminals of small fibers that are located in the area of inflammation are 
subject to an altered physical environment as a consequence of fluid extravasation. What 
effect local changes from edema may have in the responsiveness of joint receptors is 
unclear. In other preparations, edema may act to enhance or deter afferent responsiveness, 
the direction of the effect being dependent on tissue properties that are peculiar to each site 
(Cooper etal, 1990). 

Acquisition of transducing capacity could be similar to observations of recruited 
activity described by other laboratories. This "recruitment" of afferents was observed in 
the cat knee joint preparation (Schaible and Schmidt, 1985, 1988b) and also in cutaneous 
preparations (Handwerker et al., 1991). A distinction between our observations and those 
of Schaible and Schmidt is that our sensitized afferents all have some pre-existing 
reactivity. We did not observe recruitment as silent units which "wake up." Given this, 
recruited activity and acquired coding may be distinct forms of sensitization. Our failure to 
observe recruitment may be due to methodological constraints of our preparation. In our 
experiments, extracellular recordings of neural activity in the trigeminal ganglion limits the 
number of neurons that could be recorded at any site. Very few cell bodies are in the 
functional range of the microelectrode. On the other hand, in teased fiber preparations such 
as those used by Schaible, Schmidt and Handwerker, electrodes have essentially zero 
impedance, therefore many more afferents can be recorded from simultaneously. This 
makes it more likely for recruitment to be observed. 



57 



Factors Contributing to Sensirization 

Mechanical sensitization of joint afferents, following inflammation, is likely to be 
due to the production and release of endogenous substances. Injection of carrageenan 
produces a rapid inflammation that has been characterized in a number of behavioral and 
physiological preparations (Vinegar et al., 1987). Various factors may contribute to 
sensitization of joint afferents during carrageenan-induced inflammation, including both 
edema and the formation and release of algesics. 

Changes in the response properties of joint afferents during inflammation have been 
attributed to the actions of bradykinin, prostaglandins, and serotonin. These mediators 
may alter mechanical responsivity of afferents, modify chemical responsivity, activate 
afferents or a combination of the three. Changes in reactivity of small fibers in inflamed 
tissue to bradykinin have been observed (Kanaka et al., 1985; He et al., 1990; Grubb et 
al., 1991). Bradykinin activates most group 111 and IV units that responded to passive joint 
movement. Bradykinin also activates afferents otherwise classified as "silent" (Heppleman 
et al., 1987). ; 

Joint afferents can also be activated by prostaglandin (E or I). Prostaglandins Ei or 
E2 activated small afferents which responded to passive joint movement (Heppleman et al., 
1985; Schaible and Schmidt, 1988a), and modified mechanical responses of these 
afferents. Following exposure to PGE2, most group III and some group IV units showed 
enhanced joint movement reactivity and responded within the normal range of motion. 
These PGEi-evoked increases in unit responsiveness paralleled those observed during 
acute arthritis (Schaible and Schmidt, 1985, 1988a). Similar properties have been 
prescribed for PGI2, and it has been suggested that PGI2 may be the dominant PG in joint 
afferent sensitization ( Birrell et al., 1991; McQueen et al., 1991). 

Interactions between pro-inflammatory mediators are also likely to be important, but 
they have not been determined in much detail. Prostaglandin Ei (Schaible, 1983) and 



58 



prostaglandin E2 (Grubb et al., 1991) have been shown to sensitize joint nociceptors to 
bradykinin. This may impact both on movement sensitive and tonic forms of joint pain. 

Serotonin is also important in nociceptor sensitization. The effect of 5-HT on 
response characteristics of small afferent fibers have been studied in normal and inflamed 
cat knee joints (Heppelman et al., 1987) and rat ankle joints (Birrell et al., 1990; Grubb et 
al., 1988). Most group III and IV fibers that showed reactivity to cat knee movement were 
also activated by 5-HT. Units recorded from normal rat ankle joints were excited by 5-HT 
and showed enhanced activity in arthritic joints. 

The consequences of carrageenan injections are very complex, and have not been 
determined for joints specifically (Vinegar et al., 1987). One sequence of events that 
occurs in skin, during the initial stage of inflammation (0-60 min) suggests a divergence 
firom mechanisms proposed for sensitization of joint afferents. Immediately after injection 
of carrageenan, small amounts are absorbed by mast cells. The cytotoxic action of 
carrageenan initiates the arachidonate metabolic cascade and mast cell degranulation. 
Endoperoxides and serotonin are released. The endoperoxides are not believed to be 
prostaglandins but are believed to be reactive intermediates, and bradykinin is not believed 
to play a role. This stands in contrast to studies directly implicating bradykinin, PGE's and 
PGI2 in afferent sensitization and at the very least implicates that additional factors may 
play a role in carrageenan inflammation. The role of 5-HT in carrageenan induced arthritis 
is also unclear. While 5-HT is released by carrageenan in rats, it is unlikely to be directly 
released in other species due to the absence of 5-HT in mast cells. Serotonin may be more 
important when vascular damage occurs (Zeller et al, 1983; Garcia-Leme, 1989). This 
may, in fact, be more relevant to TMJ dysfunction. 

Clearly, reactivity to a host of algesics is shared by most small diameter afferents 
innervating joint tissue. Bradykinin, prostaglandins and perhaps 5-HT may play a role in 
afferent sensitization in inflamed joints. However, in each instance, it is not clear what is 
meant by normal range of motion and it is not clear to what extent shifts produced by 



59 



bradykinin, PGE2 or serotonin are the basis for changes produced with carrageenan or 
other proinflammatory substances. The lack of detail in this respect is partly due to the 
absence of quantification of stimulus and response variables. Quantification of neural 
activity in respect to threshold, range and salient stimulus features (static or dynamic 
reactivity) should permit a fuller evaluation of role played by these substances and others in 
modification of joint nociceptor reactivity. 



APPENDIX A 

DEVELOPMENTT AND MAINTENANCE OF TMJ PAIN 

Many theories have been advanced to account for the production of TMJ pains. 
(For reviews, see Deboever, 1973; Dubner et al., 1978, Yemm, 1979). TMJ dysfunction 
may account not only for pain in the joint itself, but also for pain arising from associated 
facial structures. 

Intra-articular Origins of TMJ Pain 

1) Pressure Theory 

Pressure theories have been the most prevalent explanations for the production of 
TMJ pain. These theories suggest that disruption of the normal articular mechanics may 
impose abnormal pressures on structures of the TMJ. Costen (1934) postulated that facial 
pain associated with the TMJ was a consequence of pressure on the auriculotemporal nerve 
brought about by impaction of the condyle against the tympanic plate. Anatomically, this 
theory is untenable since the auriculotemporal nerve ramifies before reaching the TMJ. The 
articular branches of the auriculotemporal nerve arise at the medialposterior aspect of the 
neck of the condyle and ascend into the soft tissue of the joint inferior to the tympanic plate. 

The auriculotemporal nerve is vulnerable to pressure at its proximal course. The 
auriculotemporal nerve arises from the posterior trunk of the mandibular nerve along the 
medial surface of the lower belly of the lateral pterygoid muscle. Entrapment of the 
auriculotemporal nerve in the lateral pterygoid muscle has been demonstrated in 5% of 



60 



61 



cadaver specimens (Loughner et al., 1990). Pressure in the form of compression by a 
hyperactive lateral pterygoid muscle may produce pain and/or paresthesia. Furthermore, 
patients with an internal derangement of the TMJ often have accompanying spasticity of the 
lateral pterygoid muscle. 

Pressure on the posterior attachment tissues by the condyle could also cause TMJ 
pain (Sicher, 1955). Posterior displacement of the condyle or spastic contracture of the 
superior belly of the lateral pterygoid muscle may result in anterior displacement of the 
disc. As a consequence, the posterior attachment tissues are positioned where forces 
generated during mastication may produce local pressure on these highly vascularized and 
innervated tissues. '-■■■ ' 

Local joint pressure may activate mechanoreceptive nociceptors in connective tissue 
such as the posterior attachment tissues. Inflammation could result from trauma due to a 
sudden, intense impact or from repeated pressure. Endogenous algesics released in the 
zone of inflammation may sensitize joint nociceptors by decreasing threshold and 
increasing response to mechanical stimuli (Heppelman et al., 1985). 

A common procedure thought to discem anterior displacement of the disc is the 
impact-loading test. Manual loading applied in an anterior- superior direction at the 
posterior portion of the body of the mandible impacts the condyle into the articular fossa. 
If pain is evoked, it is thought that the disc is displaced and the condyle is impacting onto 
the posterior attachment tissues. However, disc displacement may exist without impact 
loading pain. This is assessed by imaging techniques, such as arthrography or magnetic 
resonsance imaging. Therefore, direct pressure on the disc or posterior attachment tissues 
is not sufficient to explain TMJ pain in all cases. 

A corollary notion related to Sicher's theory was advanced by Frost (1968) to 
explain some patterns of joint pain. Frost hypothesized that bone pain may be evoked by 
the pressure of two articulating, irregular, joint surfaces in the absence of an intact 
interposing disc. Presumably, the irregular bony surfaces represent osteoarthritic changes. 






et .jlMb «.■ 



62 



Other investigators (Kreutziger and Mahan, 1975) have included arthroses of bony 
structures as causative factors in TMJ pain. Besides the degenerative processes that may 
occur in the bony anatomy of the TMJ, degenerative changes of the villi of the synovium 
have been claimed to be causally related to TMJ pain (Olson, 1969). Supposedly, 
disruption of the secretory function of the vilU can disturb proper nutrition and lubrication 
of the TMJ resulting in TMJ dysfunction. 

2) TensionTheory . 

Tension theories of TMJ pain can be divided into static and dynamic. Static state 
involves a resting position of the mandible. Dynamic state involves active or passive jaw 
movement. Anteriormedial displacement of the disc may generate static tension on the 
posterior and lateral aspects of the capsule (Dubner et al., 1978) where the greatest member 
of mechanoreceptors are located (Zimny, 1988). It is possible tiiat resting tension will 
produce prolonged discharge in TMJ nociceptors. If the anteriormedial displacement of the 
disc is advanced, tiiere is a release of tiie disc attachment at rhc lateral pole of die condyle 
which untethers the disc from the lateral aspect of the TMJ. In this case, the posterior 
attachment tissues are vulnerable to tension from a disc displacement during static 

conditions. •. 

Patients suffering from pain in the TMJ often demonstrate symptoms of capsulitis; 
tills included pain on local palpation or pain during small movements witiiin the normal 
range of motion. Inflammatory processes in the TMJ may initiate or potentiate TMJ pain 
(Dubner et al, 1978). Dynamic tiieories propose that pain is produced during jaw 
movement by excitation of functionally distinct types of mechanoreceptors in tiie capsule 
and posterior attachment tissues. Activation may be enhanced by capsulitis. Zimmy 
(1988) advanced a conceptual model of TMJ pain during jaw movement. As tiie condyle 
rotates and translates freely through intermediate degrees of angle, die capsule and posterior 
attachment tissues are deformed. Such deformation is normally insufficient to excite 
mechanoreceptors. As tiie condyle approaches its border movement, the capsule and 



63 



posterior attachment tissues become taut. Mechanoreceptors in the capsule and posterior 
attachment tissues are activated by the resultant tension. Thus, these mechanoreceptors 
appear to act as detectors that sense the safe limits of joint movement. Supposedly, jaw 
movement beyond safe limits can represent real or potential tissue damaging stimuli. If 
these mechanoreceptors are nociceptors, they may be sensitized following capsulitis so that 
small movements in the functional range of motion produce pain. Clark and Burgess 
(1975) suggested that large, myelinated afferents signal the pressure felt as the extremes of 
joint movement are reached. These investigators demonstrated that slowly adapting 
receptors in the capsule were excited only at extremes of flexion and extension of the knee 
joint of the cat (Burgess and Clark, 1969). On the other hand, Schaible and Schmidt 
(1983b) attribute a similar detection role for small fibers which are active only at the 
borders of the joint movement. 

Following capsulitis, the tension required to produce activation of nociceptors 
might be greatly reduced. Animals studies in the cat knee joint (Schaible and Schmidt, 
1988b) and rat ankle joint (Guilbaud, 1988) have demonstrated increased responsiveness 
of group ni and IV afferents to innocuous mechanical stimulation after induction of acute 
inflammation . The relationship between nociceptor discharge and capsular tension is yet to 
be demonstrated. 

The reactivity of mechanoreceptors in the capsule of the cat knee have been used to 
assess tension produced by joint movement (Grigg and Hoffman, 1989; Hoffman and 
Grigg, 1989). The frequency of neurons with receptive fields in the posterior capsule 
showed a linear relationship with tension applied (knee extension) at the area of the 
receptive field. The posterior joint capsule was minimally loaded even during 
hyperextension movements. 



64 
Extra-articular Theories of TMJ pain 

Distinct theories of the origin of extra-articular pain have arisen, and include the 
myofascial pain theory and referred pain theory. 
1) Myofascial Pain Theory 

The myofascial pain theory postulates chronic hyperactivity in head and neck 
musculature as a causative agent in extra-articular pain. The myofascial pain theory 
suggests that the chronicity of muscle pain is due to the "trigger point" (Travell, 1976). 
The trigger point is defined as a localized area of chronic inflammation of fibrous 
connective tissue in muscle. Histological examination of biopsy material from trigger 
points in patients suffering from interstitial myofibrositis reveal degranulated mast cells and 
platelet clots (Awad, 1973). The author proposes a hypothesis suggesting that trauma- 
induced extravasation of platelets leads to release of 5-HT which subsequently results in 
edema and vasoconstriction. The release of such endogenous algesics in muscle may play 
a role in the pain and tenderness associated with trigger points. For example, activation of 
group rv afferent neurons in cat muscle have been demonstrated by close arterial injection 
of bradykinin, 5-HT or histamine (Mense and Schmidt, 1974). Serotonin may also 
sensitize mucosal nociceptors to mechanical stimuli (Friedman et al., 1988; Cooper et al., 
1991). 

Muscle pain and the reduction of pain free jaw movement are fi-equent complaints of 
patients with facial pain. The limitation of jaw movement may involve the modulation of 
the reflex control of masticatory muscles (Klineberg, 1971; Dubner et al., 1978). 
Greenfield and Wyke (1966) studied the role of TMJ afferents in reflexes that modify the 
activity of muscles of mastication. The experimental procedure involved detaching all the 
supra- and infra-mandibular muscles at their insertions from one half of the cat mandible. 
Movement of the ipsilateral half of the mandible resulted in activation or inhibition of 



65 



dissected muscles. Similar responses were produced in the detatched muscles by direct 
tension on the capsule after condylectomy. 

Jaw movement has been shown to modulate the firing pattern of alpha motoneurons 
in the trigeminal motor nucleus in cats (Kawamura et al., 1967). These investigators 
demonstrated changes in the discharge rate of motor neurons of the masseter muscle in 
response to passive rotation of the ipsilateral condyle. Rotating the condyle to an open 
position evoked an increase in firing pattern of masseter motoneurons. A closed position 
evoked a decrease in firing pattern. ■ " 

Abe and Kawamura (1973) recorded efferent discharges from branches of the 
mandibular nerve which innervate the masseter and digastric muscles. Ipsilateral condylar 
rotation to an open position inhibited alpha-motor units in the masseteric nerve. Lxx^al 
mechanical stimulation of the posterior part of the TMJ capsule inhibited the discharge 
pattern of masseteric neurons and facilitated motor fibers innervating the digastric muscle. 
It is not surprising that afferent activity from mechanoreceptors in the TMJ modulate 
efferent activity in masticatory muscles in order to coordinate jaw movement. The presence 
of chronic activation of TMJ afferents may induce chronic reflex activation of facial 
musculature. Chronic activation may produce muscle pain that limits movement. 

Clinically, bruxism has been associated with muscle hyperactivity and TMJ 
dysfunction. Bruxism is defined as a nonfunctional voluntary or involuntary mandibular 
activity featuring habitual grinding or clenching of the teeth (Kawamura, 1980). Chronic, 
repetitive mandibular movement seen in bruxism is thought to deliver excessive reaction 
forces to the TMJ which could produce local inflammatory changes. Putative causes of 
bruxism include occlusal stress, CNS and hereditary factors. 
2) Referred pain theory 

Pain may be referred to the TMJ from other head and neck regions (Bell, 1969). 
Travell (1976) suggested that continuous hyperactivity of muscles from the head and neck 
may refer pain to the TMJ. The explanations for the origin of referred pain have largely 



66 



ruled out nerve branching in the periphery as a source of referred pain. The convergence 
theory of referred pain invokes a central locus of action in the superficial layers of the 
medullary dorsal horn. Noxious input from different sources converge on transmission 
cells responding to noxious input (for review, see Fields, 1987). Pain may be mistakenly 
mislocated to an area distant from the site of origin due to expectation or previous 
experience with pain in the referred site. 

In most cases, TMJ pain is not restricted to the joint but is also associated with 
extra-articular regions. The most common areas are ipsilateral eyeball, superciliary ridge, 
deep masseter muscle, and angle of mandible (Mahan and Ailing, 1991). The 
craniovertebral junction and upper neck are other referral sites of TMJ pain (Schellhas et 
al., 1989). ./ . .' , ,: 






-*. _.Hj . ^i. .^_-^ H 



APPENDIX B 



PSYCHOPHYSICS OF TMJ DISORDERS 



Pain and mandibular dysfunction are two-common manifestations of TMJ 
disorders. Pain can occur when the mandible is at rest or during function. Disordered 
movement of the mandible is a sign of mandibular dysfunction (i.e. the inability to 
masticate properly). Patients suffering from TMJ disorders often complain of pain while 
chewing. Whether mandibular dysfuntion is directiy or indirectly due to TMJ disorder or 
due uniquely to pain that results from jaw movement is unclear. 

' Chewing efficiency, jaw movement, biting force and perception of jaw position are 
quantifiable features of mastication. A review of the literature reveals studies which have 
been directed at investigating the relationship betwen TMJ disorders and mastication. 
There has been little psychophysical experimentation involved in quantifying pain 
associated with mandibular dysfunction. Even though most of these studies pertain to 
treatment efficacy, understanding the relationship between TMJ disorders and mastication 
may be valuable in understanding the relationship between pain and TMJ disorders. 

- Chewing Efficiencv 

Typically, the clinical appraisal of individual's chewing efficiency is limited to a 
subjective report provided by the patient. Early investigators (Christiansen, 1922; 
Dahlberg, 1942) developed the technique of using a series of sieves with different mesh 
sizes and test materials for chewing in order to estimate chewing efficiency. A simple 



67 



68 



method that can be used clinically to assess chewing efficiency was developed by Loos 
(1963) and modified by Carlsson and Helkimo (1972). Test material is chewed for 10, 20 
or 40 seconds. 

Masticated test materials are then measured in millimeters. Chewing efficiency is rated 
according to the size of the material and number of seconds of chewing. 

A more elaborate, standardized measure of chewing efficiency, called the 
Coefficient of Masticatory Performance, was developed by Manly and Braley (1950). The 
Coefficient of Masticatory Performance was defined as the percentage of chewed peanuts 
that pass through a 10-mesh screen sieve after being subjected to 20 masticatory strokes. 
Rominger and Rugh (1986), utilizing this test, compared the chewing performance of a 
group of patients with TMJ dysfunction to a group of normal controls. The patient group 
had significandy lower coefficient scores than the normal control group. Lemke et al. 
(1987) investigated the level of masticatory efficiency of post-TMJ surgical patients several 
years after treatment. These investigators found that the post-surgery group had 
significantly lower chewing efficiency scores than a group of non-treated non- 
dysfunctional patients. .. 

Taken together, these studies indicate a negative relationship between chewing 
efficiency and TMJ disorders. Whether the inability to chew efficiently is due to the TMJ 
pain or associated muscular pain is uncertain. ^ 

n 

Jaw Movement 

The sensory apparatus of the TMJ is thought to play a role in the synchronizing 
mechanisms involved with the control of jaw movement (Sicher, 1955). The influences of 
TMJ afferents on functional jaw movements has been studied in both normal subjects and 
patients suffering from TMJ disorders. In normal subjects, Posselt and Thilander (1965) 
anesthetized the lateral part of the TMJ capsule. They observed an increase in lateral 



m 



movement and maximum opening. The authors suggested that the lateral ligament may be 
associated with a protective mechanism during extreme opening. Klineberg (1980) also 
anesthetized the TMJs of normal subjects and observed an increase in size of the envelope 
of function (range of motion), and suggested that mechanoreceptors of the TMJ play a 
modulatory role in motor control of the mandible. 

One measure of jaw movement is maximum range of motion (ROM). The 
measurement is made for opening, lateral and protmsive excursions. An assessment of 
ROM for normal subjects has been reported by Posselt (1968). For normal subjects (adult 
males) maximum opening averages 50-60 mm; hinge opening, 20-25 mm; lateral excursion 
from midline, 10 mm; and protrusive excursion, 10 mm. Anaesthesization of the lateral 
capusle of the TMJ increased hinge opening and protrusion by 10-15% (Posselt and 
Thilander, 1965). For patients suffering from TMJ disorders, ROM is generally limited 
compared to normal subjects. Helkimo (1974) devised a pain-dysfunction index which 
rates severity of mandibular function in regard to pain report for jaw movement and TMJ 
palpation. This index was modified by Zarb and Carlsson (1988). Normal ROM was >39 
mm for opening and >6 mm for lateral excursions. For patients, ROM was 30-39 mm for 
opening and 4-6 mm for lateral excursions. Patients with this amount of impairment 
reported pain during at least one jaw movement and pain on palpation of the TMJ's. For 
other patients, ROM was <30 mm for opening and <4 mm for lateral excursions. Patients 
with this amount of impairment reported during 2 or more jaw movements and pain on 
palpation of the TMJ's. 

Many clinicians observe a decrease in ROM for patients suffering from TMJ 
disorders. These patients are often hesitant to open their mouth maximally because of real 
or expected pain. As a result, a measure of ROM may result in a value less than the patient 
is actually capable of producing. Therefore, other components of mastication may be more 
likely to be reliable measures of jaw function. Moreover, the movements of the mandible 



70 



that are made during mastication are well within the border movements of the mandible as 
defined by the ROM (Okeson, 1989). • > . 

Jaw Position 

One feature of mandibular function is the ability to control the position of the 
mandible within the limits of one's maximum ROM. An important question in the literature 
dealing with proprioception is whether position sense is signalled by joint or muscle 
afferents. Part of the literature implicates joint afferents (For reviews see Rose and 
Mountcastle, 1959; Skoglund, 1973; Dubner et al., 1978); another part of the Uterature 
implicates muscle afferents (for review, see Burgess et al., 1982). It is reasonable to 
explain joint position sense in terms of both joint and muscle afferent input. 

Jaw position sense has been studied in both normal subjects and patients suffering 
from TMJ disorders. Thilander (1961) assessed perception of mandibular position before 
and after unilateral or bilateral anesthetization of the TMJ in normal subjects. The results 
showed that subjects had more difficulty returning to an initial jaw position, following 
anesthetization. Larsson and Thilander (1964) explored the relationship between position 
sense and local mechanical pressure applied to the TMJ in normal subjects. The authors 
found that position sense was not influenced by local pressure. When the local pressure 
was reported to be painful, again position sense was not affected. However, when the 
joint was locally anesthetized, jaw position sense deteriorated. If then, local pressure was 
applied to the joint during the course of anesthesia, position sense returned to normal 
levels. Presumably, local pressure recruited muscle afferents. Input from muscle 
mechanoreceptors may have provided the sensory feedback necessary to restore position 
sense. The authors reported that ansethetization of the TMJ was performed by infiltration 
into the skin and tissues lateral to the capsule. This technique may have not anesthetized 
the TMJ completely. 



71 



Interdental thickness discrimination is one method that has been used to analyze the 
position sense of the mandible. Interdental thickness discrimination is the ability to detect 
differences in the thickness of test materials placed between opposing teeth. Caffese et al., 
(1973) studied the possible influence of TMJ receptors in tactile occlusal perception by 
assessing minimal thickness detection between opposing teeth before and after 
anesthetization of the TMJ. These authors found significant differences in threshold 
detection in the anesthetized joint compared to the normal joint. On the other hand, Siirila 
and Laine (1972) obtained different results fi-om their study of interdental thickness 
discrimination. Anesthetization of TMJ did not significantly diminish subjects' ability to 
detect differences in thickness between teeth at various degrees of mouth opening. 
Morimoto and Kawamura (1978) obtained similar results and suggested that the muscle 
spindles in the muscles of mastication are mainly responsible for size discrimination. 

If mechanoreceptors of the TMJ play a role in jaw position sense, their influence 
maybe modulated by TMJ disorders. Ransjo and Thilander (1963) studied position sense 
of the mandible in patients with TMJ disorders which were thought to be of myogenic 
origin or due to functional malocclusion. The authors assumed that functional 
malocclusion caused impairment of TMJ receptors. Position sense was found to be poorer 
for the malocclusion group compared to the normal group. Position sense of the myogenic 
group was normal. Amelioration of TMJ symptoms after treatment was accompanied by 
improvement in the perception of jaw position. This study is in accord with the previous 
work of Thilander (1961) suggesting that TMJ mechanoreceptors play a major role in the 
ability to perceive position sense of the mandible. 

A more recent study by van Willigen et al., (1986) investigated perception of jaw 
position in subjects with symptoms of TMJ disorders. They found that all subjects with 
craniomandibular dysfunction demonstrated greater mismatches of jaw position compared 
with normal subjects. On the other hand, other studies present contrasting evidence 
(Christensen and Troest, 1975; Morimoto and Kawamura, 1978; Broekhuijsen and van 



72 



Willigen, 1983; van der Berghe et al., 1987). Morimoto and Kawamura (1978) tested 
interdental thickness discrimination in 8 patients with unilateral or bilateral mandibular 
condyles that were either surgically mobilized or removed. The authors failed to observe 
any lessened capacity to discriminate thickness. These authors concluded that TMJ 
receptors were not essential to size discrimination ability. 

Broekhuijsen and van Willigen (1983) studied position sense of the mandible in 
normal subjects before and after injection of the TMJ capsule bilaterally with local 
anesthetic. Perception of mandibular position was unaffected by anesthetization of the 
TMJs. Van den Berghe et al., (1987) assessed position sense of the mandible in patients 
suffering from TMJ disorders before and after treatment. Patients' abilities to determine 
jaw position were unchanged after successful treatment. 

The relative unimportance of joint afferents in assessing position and movement is 
noted for a variety of joints. In the human knee joint, injection of local anesthetic into the 
joint does not deteriorate the subjects' ability to detect passive angular displacements of five 
degrees (Clark et al, 1979). Moreover, total joint replacement of the hip produces little 
impairment of sensations associated with joint movement (Grigg et al, 1973). 

In summary, the ability to control the position of the jaw is an important aspect of 
mandibular function. Position sense has been studied in both normal subjects and patients 
suffering from TMJ disorders. The preponderance of the evidence suggests that sensory 
input from the TMJ contributes little information in conffoUing the position of the mandible. 

Bite Force ' , 

Different parameters of bite force, such as maximum bite force, submaximal bite 
force and bite force discrimination have been investigated in an effort to assess mandibular 
function. 



■■-■■■ J - . - .' ,r 

'■■'.': Maximum Bite Force 

The maxmum bite force is the measure of the greatest force which an individual can 
produce by biting on an instrument containing a force transducer. The maximal level of 
bite force that an individual is capable of producing is rarely required or utilized during 
chewing. Therefore, the relevance of maximum bite force as a measure of mandibular 
function is uncertain. Also, a measure of maximum bite force may result in a value less 
than an individual is capable or willing to produce. Clark et al., (1984) reported that the 
maximum bite force of normal subjects is limited by pain tolerance. Patients suffering from 
TMJ disorder may be incapable of producing maximum bite force due to the direct effect of 
mandibular dysfunction or unwillingness to bite normally due to the indirect effect of pain. 
Such may be the case in several studies that assessed maximum bite force in patients 
suffering from TMJ disorders (Helkimo et al., 1975; Sheikolelam et al., 1982). Helkimo 
et al. (1975) reponed that maximum bite force was lower in a patient group with TMJ 
disorders than for a control group. Patients' level of maximum bite force increased 
following treatment. Sheikolelam et al., (1982) observed that maximum bite force was 
significandy less for their patients with TMJ disorders than for normal controls. 

Submaximal Bite Force 

One imponant component of the normal chewing cycle is the individual's ability to 
produce and control relatively low levels of biting force. Submaximal bite force is the 
measure of different levels of biting force below maximum bite force. It seems reasonable 
to suggest that impaired mandibular function may result in impairment of the ability to 
control submaximal bite force. Several studies have investigated submaximal bite force in 
patients with mandibular dysfunction (Helkimo et al., 1975; Agerberg, 1988). Bite force 
was registered with different types of bite beams incorporating a force transducer. A 
common feature of patient populations was pain in the TMJ. These studies reported that 



74 



patients had lower values for submaximal bite force (3-25 kg) compared to control subjects 
(5-50 kg). 

Bite Force Discrimination 

In order for an individual to control the different levels of bite force, he/she must be 
able to discriminate differences in the intensity of their own biting force. The role of TMI 
mechanoreceptors in bite force discrimination has been investigated in normal subjects 
(Williams et al, 1984; Williams et al., 1989). Bite force was assessed before, during and 
after anesthetization of the TMJ by auriculotemporal nerve block (Williams et al., 1984) or 
infiltration into the superior joint cavity (Williams et al., 1989). These studies suggest that 
the TMJ mechanoreceptors do not appear to be responsible for discrimination of bite force. 

In summary, maximum bite force, submaximal bite force and bite force 
discrimination are three commonly used measures of mandibular function. Studies 
assessing maximum and submaximal bite force indicate that patients suffering from TMJ 
disorders have decreased bite force strength. The ability to discriminate bite force levels 
has not been studied in patients having TMJ disorders. Neither maximum bite force, 
submaximal bite force nor bite force discrimination measures have provided clear 
information on the relationship between TMJ sensory input and mandibular function. 



'':.,** >• i ' 



APPENDIX C 



! -I 



^fEUROANATOMY OF THE TMJ 

Until Thilander's (1961) comprehensive, anatomical and histological study of the 
innervation of the human TMJ, research on innervation of the TMJ involved macroscopic 
studies. Riidinger (1857) observed that the auriculotemporal nerve coursed to the posterior 
aspect of the joint where three or four articular branches entered the capsule. The anterior 
aspect of the capsule received one or two twigs derived from the masseteric and deep 
temporal nerves. Textbooks describing the TMJ generally accepted Rudinger's findings. 
Moreover, other anatomists (Guerrier and Bolonyi, 1948; Baumann, 1951; Hromada, 
1960) are in agreement with the neural topography described by Rudinger but for the 
possible exception of the contribution of the facial nerve. 

Some sensory fibers travel in the facial nerve, which is otherwise devoted to motor 
function. These afferent fibers constitute about 15% of the total nerve fiber population 
(Foley, 1960). Guerrier and Bolonyi (1948) reported that branches of the facial nerve 
always terminated in the lateral surface of the TMJ. Hromada (1960) stated that a twig 
fi-om the facial nerve passed into the lateral aspect of the capsule in about half of his 
dissected specimens. On the other hand, Thilander (1961) reported that, immediately 
lateral to the capsule, a twig from the facial nerves courses in an anterior direction but does 
not ramify into the joint. Kerr (1962) also reported that afferents of the facial nerve 
terminate only in the dermatomes of CI and C2 in the cat. Our observations (unpublished) 
suggest that the facial nerve does not innervate the TMJ of the human. However, the facial 



75 



76 



nerve was seen to communicate with the auriculotemporal nerve distal to the TMJ. 

In contrast to the innervation of the human TMJ, the facial nerve of the goat 
communicates with the auriculotemporal nerve proximal to the articular branches. The 
functional implications of this topography are unclear. Some afferents from the TMJ may 
travel centrally in the facial nerve or afferents in the facial nerve travel in the 
auriculotemporal nerve. 

Thilander (1961) reported that the auriculotemporal nerve is the major sensory 
nerve of the TMJ. The branches from the auriculotemporal nerve innervate the posterior, 
medial, and lateral aspect of the anterior capsule. These branches enter the inferior aspect 
of the capsule along the neck of the condyle. This observation is not in accord with 
Rudinger (1857) who reported that the articular branches of the auriculotemporal nerve 
passed between the condyle and the pars tympanica. However, a recent study (Loughner et 
al., 1990) confirms Thilander's report. In this laboratory, macroscopic dissections of the 
TMJ of the goat (unpublished) show a similar course of the auriculotemporal nerve and 
distribution of articular branches. 

According to Hilton's Law (1879), nerves that innervate the muscles that move a 
particular joint also contribute to innervation of the joint. Surprisingly, that contribution is 
only about 30% of die total TMJ innervation (Thilander, 1961). Twigs from the masseteric 
nerve innervate parts of the anterior capsule and anterior aspect of the medial capsule. The 
posterior deep temporal nerve innervate the lateral anterior aspect of the capsule. The 
auriculotemporal nerve supplies the remaining 70% of the TMJ. 

Thilander (1961) estimated that the human TMJ is innervated by an average of 1500 
peripheral afferent fibers. The auriculotemporal nerve contributes two thirds of the total 
amount. The greatest number of the articular fibers have a diameter between 1 and 2 fxm 
and probably terminate as free endings in the capsule, posterior attachment tissues and 
adventitia of blood vessels associated with the joint. Other afferent fibers, though fewer in 
number, and ranging from 6 to 1 1 fim, terminate in complex neural endings. 



77 



The posterior attachment tissues contain a rich plexus of nerve fibers from the 
auriculotemporal nerve. Hall et al., (1985) identified and quantified the types of nerve 
fibers in the posterior attachment tissues. The authors found that the majority of axons 
were unmyelinated. The lateral portion of the posterior attachment tissues contain 
significantly higher percentage of unmyelinated fibers. Other investigators (Weinmann and 
Sicher, 1951; Sicher, 1955) have reported abundant innervation in association with blood 
vessels in the loose connective tissue between the posteror border of the articular disc and 
the capsule. 

A few nerve fibers have been observed in the synovial membrane of the human 
TMJ (Thilander, 1961; Ishibashi, 1966). Ishibashi, (1974) found free nerve endings and 
glomerular endings beneath the superficial cell layer of the synovial membrane located on 
the posterior aspect of the TMJ. Bemick (1962) described encapsulated end bulbs in the 
synovial folds in the TMJ of the rat. These observations appear to contradict those who 
believe that the synovial tissue serves no sensory function (Olson, 1969). Although the 
nerve endings in the synovial membrane have been reported to be closely associated with 
blood vessels (Hagen-Tom, 1882; Davis, 1945), unmyelinated nerve fibers have been 
described in the synovium separated from blood vessels (Kellgren and Samuel, 1950; 
Rossie, 1950). Kawamura et al. (1967) found Golgi-type endings in the synovial tissue 
layer of the TMJ of the cat but not in the synovial membrane itself Whether the synovial 
membrane is innervated or not, the justapositon of afferent fibers allows sensibility in the 
territory of the synovium. 

As reported by Thilander (1961), the articular disc contained no nerve endings. 
However, other investigators (Ishibashi, 1966; Schmid, 1969; Zimny and St. Onge, 1987) 
described articular nerves innervating the periphery of the disc in the human TMJ. Similar 
results were reported in the monkey (Keller and Moffet, 1968), in the rat (Bernick, 1962) 
and in the mouse (Frommer and Monroe, 1966). These studies are consistent with 
histological studies of fetal material. Kitamura (1974) reported that, in the 5th month in 



78 



utett), nerve fibers were observed in the disc; further development was accompanied by a 
reduction in disc innervation. Corroboration of the influence of growth on disc innervation 
came from Hromada (1960), who observed free nerve endings in the disc of various 
animals; at older ages such endings were limited to the periphery of the disc. By 
comparison, the nerve supply to the meniscus of the human knee remains unclear (For 
review see Zimny, 1988). The most recent study (Albright and Zimny, 1987) reports that 
free and complex nerve endings were observed in outer and middle one-third of the 
meniscus; whereas, no innervation was found in the inner one-third. 

Innervation of the TMJ of the monkey and cat resemble that of the human joint 
(Franks, 1965; Keller and Moffett, 1968). Branches from the deep temporal and 
masseteric nerves supply the anterior capsule, and the articular branches of the 
auriculotemporal nerve supply the TMJ posteriorly. Preliminary macrodissection of the 
nerves innervating the TMJ of one goat was performed in this laboratory. The 
auriculotemporal nerve gave off three articular branches along the posterior aspect of the 
neck of the condyle. The articular branches ascended into the fatty and fibrous articular 
tissue. The termination of the temporal branch of the auriculotemporal nerve appeared in 
the facial skin inferior to the zygomatic arch. The masseteric nerve was observed to arise 
from the anterior trunk of the mandibular nerve, course lateral along the anterior border of 
the capsule of the TMJ and terminate in the superficial and deep masseter muscle. Twigs 
from the masseteric nerve appeared to enter the anteriorlateral aspect of the capsule. 

Tissues surrounding articulations possess fewer types of receptors than muscle or 
cutaneous tissue. Thilander (1961) described four types of neural endings in the human 
TMJ: Ruffini-like receptors, modified Pacinian endings, Golgi tendon organs and free 
nerve endings. Ishibashi (1966) also reported the presence of free nerve endings and 
complex terminal expansions in the human TMJ. Keller and Moffett (1968) reported free 
and complex nerve endings in the TMJ of monkeys. Many investigators have identified 



n 



free and complex nerve endings in the TMJ of the cat (Kawamura and Majima, 1964; 
Greenfield and Wyke, 1966; Kawamura et al., 1967; Wyke, 1967; Klineberg, 1971). 

The three types of complicated nerve endings were sparsely distributed compared to 
the free nerve endings. The most common complex ending is the Ruffini ending. Ruffmi- 
like endings were encountered in the lateral and posteriorlateral aspect of the capsule in 
humans (Thilander, 1961). Griffin and Harris (1975) described a thinly unencapsulated 
corpuscle located close to the periosteum of the neck of the condyle and in the lateral and 
medial aspects of the capsule fat pads. These receptors may have been similar to the 
Ruffini endings described by Klineberg (1971) in the TMJ of the cat. The Ruffini-type, 
low theshold mechanoreceptors were once thought to signal joint position (Boyd and 
Roberts, 1953; Boyd, 1954; Cohen, 1955; Skoglund, 1956, 1973). However, other 
investigators (Burgess and Clark, 1969; McCall et al., 1974; Clark and Burgess, 1975; 
Clark, 1975; Grigg, 1975; Grigg and Greenspan, 1977) have shown that Ruffini endings 
are seldom active at intermediate positions of the cat knee joint. They are responsive to 
extremes of joint movement. Consequently, these receptors are unlikely the peripheral 
neural substrate that code for position sense. Instead, Ruffini endings appear to signal the 
torque produced when the joint is extended and/or rotated at the limit of the range of 
motion. (Grigg et al., 1982a). 

Pacinian endings were found in the lateral aspect of the capsule (Thilander, 1961). 
Paciniform-tyf)e end organs in cats have a similar distribution as Ruffini endings but less 
dense (Kawamura et al., 1967; Klineberg, 1971). Golgi tendon organs were located in the 
temporomandibular ligament and anterior capsule (Thilander, 1961; Griffin et al., 1965). 
In the anterior capsule, the Golgi end organ was in series with the extrafusal fibers of the 
lateral pterygoid muscle and tendon fasciculi of the capsular tissue or the fibrous tissue of 
the pes menisci. In the temporomandibular ligament the Golgi end organ was thought to be 
in series with fibers of the deep masseter muscle. Both Paciniform endings and Golgi 
tendon organs are thought to respond like comparable endings found in cutaneous and 



80 



muscle tissue (Willis and Coggeshall, 1978). However, Grigg et al., (1982b) showed that 
in the cat knee, Golgi tendon organs responded to local pressure applied perpendicular to 
the capsule but not to tension applied parallel to the capsule. 

Free nerve endings are the most abundant receptor in the capsule of the human 
TMJ. Presumably, free nerve endings derived from myelinated afferents subserve fast pain 
sensibility and nociceptive somatic reflexes; free nerve endings derived from unmyelinated 
nerve fibers may subserve slow pain sensibility or innervate vascular elements. Free 
ending receptor specializations have yet to be defined. In sympathectomized cats, sensory 
nonmedullated plexuses have been found in the inner layers of the fibrous capsule, adjacent 
synovial tissues and adventitia of blood vessels in the knee joint of cat (Samuel, 1952). 
Free endings have been described in the joint capsule, joint ligaments and periarticular fat 
pads (Greenfield and Wyke, 1966). Similar results have been reported by Freeman and 
Wyke (1967). Free endings characteristic of group III and IV afferents have been 
described in the Archilles tendon of the cat as well (Andres et al., 1980). Some of these 
free endings may be nociceptors. 

Although there are great variations in the morphology of the TMJ between species, 
the innervation of the TMJ is quite similar (Kawamura, 1980). The distribution and 
appearance of receptors may vary with age and species (Polacek, 1966), but the types of 
receptors are consonant across species including human. 

In summary, the mammalian TMJ contains four types of receptors (for review see 
Skoglund, 1973; Zimny, 1988). The Ruffini and Paciniform mechanoreceptors are 
innervated by medium-sized (Ab) myelinated fibers, the Golgi tendon organ by large (Aa) 
myelinated fibers and the free endings by fine myelinated and unmyelinated afferents. 



a- , y 



APPENDIX D 
CENTTRAL REPRESENTATION OF TMJ AFFERENTS 

The central distribution of TMJ afferents has been studied in the trigeminal nuclear 
complex. The main sensory nuclei and the dorsal part of the rostral spinal nucleus were 
found to contain neurons responsive to isolated condylar movement or pressure applied to 
the joint capsule of the cat (Kawamura aand Majima, 1964; Kawamura et al., 1967). The 
authors reported simple, qualitative findings describing three types of responses to 
ipsilateral condylar rotation (rapidly adapting, slowly adapting and on-off types) and two 
types of responses to mechanical stimulation (rapidly adapting and slowly adapting types). 
In addition, response patterns of neurons in the trigeminal motor nucleus were recorded 
during condylar movements or mechanical stimulation of the joint capsule. As with 
responses from the sensory nuclei, no quantification of activity was attempted. Procaine 
infiltration into the joint capsule abolished neural responses. Another qualitative study 
reported unit activity found in the trigeminal main sensory nucleus and nucleus oralis of the 
cat that responded to jaw rotation or pressure applied to the ipsilateral TMJ (Sessle and 
Greenwood, 1976). One of these units was antidromically activated from the thalamus. 
Other direct projections from the superficial layers of the medullary dorsal hom to the 
thalamus have been demonstrated anatomically (Craig and Burton, 1981) and 
electrophysiologically (Dostrovsky and Broton, 1985). 

The caudal aspects of the trigeminal nucleus complex were found to contain 
neurons that are driven by electrical, mechanical, and algesic chemical stimuli applied to the 
TMJ (Broton and Sessle, 1988). Neurons in the subnucleus caudalis were first classified 



81 



a 



on the basis of their responsiveness to mechanical stimulation to the skin: low-threshold 
mechanoreceptors (LTM), wide dynamic range (WDR) or nociceptive specified (NS). 
WDR and NS neurons responded maximally to algesic chemical and intense mechanical 
stimulation applied to the joint. TMJ stimulation consisted of local probing or extreme jaw 
opening. The majority of single units with TMJ input received convergent input firom 
cutaneous afferents. Kojima (1990) also found convergence patterns of afferent input from 
the TMJ and muscle in the subnucleus caudalis. Most of the units tested were responsive 
to mechanical and thermal stimulation of both the TMJ and the masseter muscle. 

Extensive convergence of cutaneous and muscle inputs on second-order neurons 
that respond to articular movement have been described in the cat knee (Schaible et al., 
1986). In some neurons, maximal responses to joint movement occurred with forced 
extension, inward rotation or outward rotation. Other neurons were excited only by 
noxious movement. Joint movement was considered noxious if the movement was made 
forceably. No quantification of forces was attempted. This report compares favorably 
with the effects of TMJ stimulation in neurons in the medullary dorsal horn (Broton and 
Sessle, 1988), in that most second order neurons that respond to noxious joint simulation 
also receive convergent input from skin and/or muscle. Such central convergence may be 
important in explaining the tendemess of skin and/or muscles near the joint that are often 
observed clinically when the joint is painful. 

Changes in responsiveness in spinal neurons have been investigated during the 
development of acute arthritis in the cat knee jont (Neugebauer and Schaible, 1990). AH 
neurons tested with joint input showed enhanced responsiveness to joint flexion after 
induction of inflammation. 

Other electrophysiological experiments performed in polyarthritic rats demonstrated 
nociceptive inputs from chronically inflamed joints to the ventrobasal thalmus (Guilbaud et 
al., 1980; Gautron and Guilbaud, 1982), intralaminar and medial thalamus (Kayser and 
Guilbaud, 1984; Dostrovsky and Guilbaud, 1990), and somatosensory cortex (Lamour et 



83 



al., 1983). One consistent feature of the neuronal reactivity seen in all of these studies is 
the increase responsiveness of central neurons to non-noxious stimulation of the inflamed 
joints. The central mechanisms which might contribute to changes in responsiveness of 
central neurons in arthritic rats is still in question. The alterations in discharge behavior 
seen in CNS neurons is likely due, in part, to the changes in responsiveness of joint 
receptors due to inflammatory processes. 



APPENDIX E 



TRIGEMINAL GANGLION 



The trigeminal ganglion is situated near the apex of the petrous bone in the middle 
cranial fossa. It lies in Meckel's cave near the cavernous sinus and internal carotid artery. 
The sensory root (portio major) enters the pons in association with the motor root (portio 
minor), which courses dorsomedially, and terminates in the trigeminal nuclear complex. 

Sensory input from the face enters the trigeminal ganglion via the opthalamic, 
maxillary and mandibular division of the trigeminal nerve. The cell bodies of these afferent 
fibers are segregated into discrete clusters (Jerge, 1964; Kerr, 1962). 

Retrograph transport of HRP injected into the cat TMJ showed that sensory 
neurons originate in the trigeminal ganglion (Romfh et al., 1979; Capra, 1987). Whether 
all of the cell bodies of afferent neurons innervating the TMJ are located in the trigeminal 
gangUon remains unanswered. There is evidence suggesting that the peripheral spinal 
neurons innervate the TMJ. Widenfalk and Wiberg (1990) injected HRP into the TMJ of 
rats. Labeled cells were observed ipsilaterally in the second to fifth dorsal root ganglion. 
In addition, there is evidence suggesting that the mesencephalic nucleus contains cell bodies 
of neurons that terminate in the TMJ. In a preliminary communication, Limwongee (1986) 
reported injection of HRP into the TMJ of rat, cat and monkey. He found labeled neurons 
in the mesencephalic nucleus at the level of the caudal pons. On the other hand, Corbin 
(1940) ablated the mesencephalic nucleus and examined histologically the auriculotemporal 
nerve. He found no degenerated fibers. In addition, Chen and Turner (1987) injected 



84 



85 



» J- N% 



HRP into the TMJ and insertion of the lateral pterygoid muscle of rats. They found no 
central projection to the mesencephalic nucleus. ,. 

Somatotopy 

There is general agreement that the trigeminal ganghon in cats is somatopically 
represented from a medial to lateral direction (Beaudreau and Jerge, 1968; Zucker and 
Welker, 1969; Kerr and Lysak, 1964; Darian-Smith et al., 1965; Marfurt, 1981). The 
ophthalmic division lies anteriomedially, the mandibular division lies posteriolaterally and 
the maxillary division is situated in an intermediate position. Overlap between divisions 
has been reported (Marfurt, 1981; Henry et al., 1986). Romfh et al., (1979) and Capra 
(1987) reported that injection of HRP into the capsular tissues of the TMJ in the cat resulted 
in a restricted distribution of label in the posteriolateral position of the trigeminal ganghon. 
Very few labeled cells were found in the most dorsal or in the most ventral areas of the 
mandibular division of the trigeminal ganglion. The majority of labeled cells is found 
throughout the intermediate zone in the posteriolateral part of the ganglion. 
Electrophysiological studies in cats (Capra and Gaitpon, 1981) and in rabbits (Lund and 
Matthews, 1981; Appenteng et al., 1982) confirmed that TMJ afferents were located in the 
posteriolateral region of the trigeminal ganglion. 

In addition to the mediolateral somatotopy , studies suggest a dorsoventral 
somatotopic organization (Kerr and Lysak, 1964; Marfurt, 1981; Capra, 1987). 
Representation of oral and perioral structures appear ventral in the ganglion. Areas remote 
from the mouth lie in the dorsum of the ganglion. 



APPENDIX F 



GROSS ANATOMY 



The TMJ in mammals is a ginglymus-arthroidal joint, i.e., a hinge joint capable of 
gliding movement (Figure F-1). The craniomandibular articulation involves the condyle of 
the mandible juxtaposed with the articular surface of the squamous portion of the temporal 
bone. Interposed between the condyle and the articular fossa is an articular disk dividing 
the articular space into upper and lower compartments. 

The periarticular soft tissue consists of fibrous capsule, posterior attachment 
tissues, synovial membrane and accessory ligaments. Except for the synovial membrane, 
these tissues serve to limit the range of motion of the joint and to maintain a packed position 
(Sicher, 1960; Rocabado, 1983). A packed position is the condyle-disc-fossa relationship 
which juxtaposes these TMJ elements at rest and during mandibular movements. The joint 
capsule is loose and composed of dense connective tissue with a collagenous matrix richly 
supplied with blood vessels and nerves. The dense connective tissue of the capsule is 
located primarily on the lateral and medial aspect of the joint and intimately associated with 
the temporomandibular and sphenomandibular ligaments, respectively. The anterior 
capsule arises ftx)m the suture line between the greater wing of the sphenoid bone and the 
temporal bone. It inserts on the anteriorlateral aspect of the condylar neck. The loose 
connective tissue of the capsule encompasses the joint posteriorly. It arises from the tragal 
cartilage laterally and tympanic plate medially. The posterior capsule, as a meshwork of 
unorganized collagen fiber, inserts and blends in with the posterior periosteum of the 
condylar neck and upper capsule of the parotid gland. 



86 



t7 



SAGITTAL VIEW 



2 .4 




1. Articular Surface of Glenoid Fossa 15. Auriculotemporal Nerve 



2. Superior Cavitt 

3. Disc (Stippled Area) 

4. Capsule 

5. Articular Surface of Condyle 

6. SjTiovial Membrane 

7. Squamo-Tympanic Suture 

8. Spine of the Sphenoid 

9. Vascular Knee of Meniscus 

10. Pes Meniscus 

11. Superior Belly of Lat. Pterygoid 

12. Inferior Belly of Lat. Pterygoid 

13. Superior Stratum of Bilaminar Zone of Meniscus 

14. Inferior Stratvun of Bilaminar Zone of Meniscus 



16. Bloodvessels 

17. Posterior Deep Temporal Nerve 

18. Squamo-Sphenoidal Suture 

19. Parotid Gland 

20. Sphenomandibular Ligament 



Fig\ireF-l 

Schematic diagram of the human temporomandibular joint. Sagittal and 
frontal views. 



88 



The dense connective tissue of tiie capsule reinforces the lateral position of the TMJ 
and is incorporated into the temporomandibular ligament. Horizontal fibers of the 
temporomandibular ligament restrict posterior displacement of the condyle and oblique 
fibers tend to limit lateral and inferior displacement (Sicher, 1960; Griffin and Malor, 
1974). The posterior attachment tissues consists of collagenous and elastic connective 
tissues which extend from the posterior border of the disc to the tympanic plate. 

Macroscopic dissections of the goat TMJ were performed in this laboratory. The 
articular surface of the condyle is oval in shape, its longer dimension is concave 
mediolateral and the shorter dimension is convex anterioposterior. The articular disc is 
ovoid, biconcave, and divides the joint into two synovial cavities. The fibrous capsule is 
moderately loose which allows for extensive lateral translation of the condyle. The capsule 
surrounds the joint, with the exception of the anteriomedial portions, where the lateral 
pterygoid muscle attaches to the neck of the condyle. With four exceptions the gross 
anatomy of the goat TMJ is similar to the human. First, the lateral aspect of the posterior 
attachment tissue extends posteriorly beyond the postglenoid process and attaches to the 
inferior surface of the zygomatic process of the temporal bone. This anatomical variation is 
associated with the lateralization of the bony articulation of the TMJ beyond the cranial 
base. Second, the articular surface of the glenoid fossa is slighdy convex in all directions, 
rather than concave. To accommodate this convexity the condyle is appropriately concave 
along the mediallateral axis. Third, there is no articular eminence. Finally, the lateral 
pterygoid muscle attaches to the anteriormedial aspect of the neck of the condyle in a 
manner similar to the human, but it does not appear to attach to the disc. 

Comparative Anatomy 

According to the classification of TumbuU (1970), goats are section 11 herbivors 
while humans are section 111 omnivores. The TMJ of the goat has been used as an animal 



t9 

' '■' ■ '■ , - I ^ 

model for oral surgery procedures because the anatomy and biomechanics are similar to the 

human TMJ (Bifano et al.. 1990). 

First, for the vertebrate chewing apparatus, the range of motion is generally 
confined to those movements necessary for dealing with a particular diet. Due to a coarse 
diet of vegetation, ruminants possess a greater range of mandibular movement than do 
carnivores. The excursive movements include hinging, lateral translation, slight protrusion 
and mediolateral shift. Hinge opening and lateral translational movements are required for 
forceful grinding. The lateral pterygoid muscle is the prime mover of the mandible during 
lateral translational movements. The lateral excursion, initiated by contraction of either one 
of the lateral pterygoid muscles, is a prerequisite to an effective grinding stroke. Both the 
goat and human possess a well-developed, lateral pterygoid muscle. 

Second, the elevated position of the condyle of the mandible relative to the occlusal 
plane benefits the operation of the masseter and medial pterygoid muscles. They function 
synergistically to provide powerful bite force needed for grinding activity. 

Third, the condyle is convex anteriorposteriorly, which allows some translation 
along a convex articular surface of the fossa. Such anteriorposterior translation represents 
a common denominator between the TMJ of non -carnivorous mammals and the human 
joints. In contrast, carnivores have a deep concave articular fossa that allows only hinge 
movement and prevents dislocation during seizure of prey. 



APPENDIX G 



SUMMARY TABLES OF TMJ REACTIVITY 



■ ^ ' V ■■I * 



:*^' 



.i C'.. 



90 



91 



CV 

(m/sec) 


r^r^'^-^-^-^Tt «n«o 


ooooooo r- r~ 


SS 


vqvqoooooTfTfOO'>*'^_vovqvo\ooooTf':t^>n 
c<^roodoccx3o6o6u^iovovduS>ocn(^c<^r<^o\0\0>owSuSr^'>o>n^ 




^a\>o^ommoo-<*-^ONOc<^vo^c<^-^io\omo^oooooN 

ooooooooooooooooooooooooooo 


1 


c<^ONU^r<^u-)0^rO'--<OvOrtr<-ic<-ioooqoooo\'--;csaNOOc^ 
Tj-' Tt vo ^' (ri vc> vd H oi vo en c<S en r-^ CS CO Tt r4 H '^' ro CS C7\ -rf vo ^^ 


FREQ. 

ASYM. 


C/5 C/5 C/3V5 C/5C/5e/2V5 

Z. Z^. Z. Z^Z. Z^^ZZo zzzzz. z^zz 

o*oo\^o>ovo,-iocsocsooZoN>ncsoovc)vot^{Scscnoovoo 
r<^cS'— lON-Hr-i.— .c<-iC3NVO'— ics— iTtcsvo^ooosor^-^cs-HTtcnr- 

•-yeses'— 1 cs ^_i ^ 


ACT. 
THRES 


z. z^, z, z^Zo zzzzz. zzzzz, z^z^ 

-^Tfmvor^ovocorj.— ioocscso»ooooo\oo«Ot— iioooocs^ 
--" — 1 '-< ^ r-( '■^ -^ CO -^ cs -^ CO ^ c<^ cs lo cs -H '— 1 r<^ — c — 1 


FREQ. 
IHRES 


Z Z 17 

r- '-1 00 cs 


00 


W ^ tL, > ^ tL, P-i > Uh _H W > tU > tL, _^ U- > PL, fc > ^ PL, > Ph > 


o 

Z 

£ 


vOTtcSO\>opO>OoqOOp-^_Ot~-;pO'--;^r--;WooovOCSu-)oo 
r-^o6^'csuS'-Hr~^wS'^'^^r~^vdr-^r~^t^ONod-rt<or-^Tt^o\r~^\dTf 

+ + + + + + + + + + + + + + + + + + + + + + + + + + + 

p[HpLHWCpLHpL,f^pL,pL,gL,pHpUPtHptH[I-WP:HpUp:.CUHCpLHpL,PL,pHC 
CCCJCC'^CCCCCCCCCCCCJCJCCCCJ 

'-<^coc5<-<'uouo'-HOfnuooc)fS^o\o^oo^ovd^'c5cDCD 

I 1 ( 1 1 1 1 1 1 1 1 1 I 1 1 1 1 1 1 1 1 1 1 1 1 1 t 

II II II II II II II II II II II II II II II II II II II II II II II II II II II 

'c'c'c'c'c'c'c'c'c'c^c'c'c^c'c'c'c'c'c'c'c'c'c'c'c'c'c 




cocorocornr<-)ror^t;:;i£^;-i'-<cSCS(S(S(NCScNrocOrn'-:'-:^^ 

pjpqc/2c/2onHH^ZffiffiQQWPUQpqpQpqpL,Jjn^<<00 


E 


pgpjoooo^HH^ZffiKQQWpqQWpqpjwjj^<<Oa 

^— (0000000000000000000000--I— ''-' 
.— i^hOOOOO"— 1.— icSCSCSCSOOOO'— '>— 1>— i^^^H.— iT^OCSCS 







92 



I 

O 

s 

< 



W 
ID 

CO 
CO 

p 

O 
Z 





CV 

(m/sec) 


<r> <o in 








S >^ 


>oo>ou-)in«o>npppppppp^«n«nvqvqininp>ovq 
odiooc5o6uSuSuSvovo\ooso\uSwSio<T)>oin(^co«/S«/SoN'nfo 






roor-cNor~r~r~'^'n^o>oO'^coc<-ivot~~oo<No\ooNt-~ 

00CD0000000CD0000000C)0C50000 




HH 


<nfooocovot^ooTt>or--ooo\ON<sooT}-cS'— ivooot^O>no\co 




Or0fSCSCN(NC^lO4fSm(N(N(Nmcnc<-l'<*'!tC<^C0Tl--<:tC0(N(S 




FREQ. 
ASYM. 


zzz^zgzzZzzz^^zzzzz^zzzzz 




ACT. 
THRES 


2: Z^Z;^^Z4£ z^zz zzzz z: z z 

S;7"^^'^'^'^PZZ'^'-'^'-5ZZ'-5'-?'-5^Z'-5'^Z^ 
^o^'-<ooiO^^<NOOst~4r-^r4csoo>ovd>OTf'o^^coco 


3 


FREQ. 
THRES 


Z ZZZZ 

p P . ."O . . . .P . . . .P 

CO vd ' ' -^ ' ' ' ' vd ' ' ' ' fs 




H 

00 


ooQQEjL,Q[l,ooQp-,ooQpL,Ppu,ooQQpL,QooQt,QQQ 


f- 


Z 

o 

u 

z 


•-<op-^_oooqt^oo-^cnr--Ttpr~;r}-_pr~;0\vopovpco«noN 

ioioioco'rfcoodTtrtvd-<:fror-^-^'o6-rtuSTr'<:tuovdw^ 

t— < 

+ + + + + + + + + + + + + + + + + + + + + + + + + 

Ph U, U, Pu U-t Uh ti< 

UHtL,tUtL.tL,tUtt,pH CtL.tL,U.tL,tU,tU,tL, C C C CfctLitL- C C 
CCCCCCCCJCCCCCCCJJJJCCCJJ 

■^■^ocor-(Noor-~m(S>o-^c<-)cnTtO"*^cocooo<sr~r~;'^ 

^CD^'oOO'-'CIJCJ'-HOCD'-'O'-JfOOOCDCDOOOcJo 

1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 

II II II II II II II II II II II II II II II II II II II 11 II 11 II II II 

"c'c'c'c'c'c'c'c'c'c'c'c'c'c'c'c'c'c'c'c'c'c'c'c'c 






<<<<<<muuQ<<<<0Q<QQQpa2;2;<<E 






CR CN CN ^ On On On On On 0\ On On On On On On On 0\ On On On On On On 0\ 
vOQNONO\NONO^^^NOrOcoOOOcOcOcoOOOOOOTi-vor~ 

<N'^(N<S^^'— i"— '>— I-— i"— i^^"— i(NfNrv)rococococncom'^t^ON 

o^^^ooooooooooooooooooooo 






^(NcocoTtTt-rj-ioioiovoNOr-r-r-oooNONOO'-H^fSro-n- 



93 






^ 




^_^ 












o 












u 












Be 


' 


• 


* 


• 


• • 


(i, '^ 


m 


m 


>o 


>n 


U-) m 


d2<^ 


«o 


>n 


«n 


»n 


in »o 




m 


^ 


oo 


o 


NO c^ 


<N 


ro 


On 


en 


r- 


<N On 


oi 


o 


O 


O 


o 


o o 


P^ 


ON 


O 


o 


r~- 


CN VO 


"^ 


CO 


VO 


<o 


(N 


(N NO 


cy? 










c« 


w>^ 


Z 


Z 


z 


Z 


^ z 


E< 


OS 


(N 


NO 


r- 


O rj- 


r-H 


t-H 


CN 


^— < 


>0 '-' 


ACT. 
THRES 


p 
od 


z 

p 

On 


z 


Z 

o 


2.0N 
9.0N 


REQ. 
HRES 


• 


. 


z 


. 


• in 


U,H 












H 














tu 


P-, 


fc 


PL, 


> l^ 


n 


P 


OD 


« 


Uh 00 




CO 


CO 


'^ 


00 


^ o 




ly-) 


oo 


O 


r- 


CO CO 


z 


+ 


+ 


+ 


+ 


+ + 


o 


Uh 










»— H 


c 


Uh 


Uh 


Uh 


Uh Uh 


H 


, 1 


C 


c 


c 


c c 


f) 


0\ 


J 


J 


J 


hJ J 


z 


>o 


•— ' 


CN 


o 


CO O 


e 


o 

1 


1 


(N 


(N 


o ■* 


II 


II 


II 


II 


II II 




c 


c 


C 


c 


c c 




-J 


J 


J 


J 


J J 




(N 


CN 


CO 








m 


< 


o 












<N 








PQ 


< 


o 


HH 


1— ( 1— > 


H 


t-H 




^-^ 


j-^ 


1 — t 1 — * 


On 


s 


On 


On 


On On 


CO 


-* 


"* 


^ ^ 


u. 


T— < 




fN 


<N 


fS CN 


CO 


s 


-^ 


^ 


■^ Tf 




O 


O 


O 


o o 




»-H 


<N 


CO 


■^ 


Tf ^ 



94 



CV 

(m/sec) 








oopooooppppp 


7^ 

if 


rl >0 t^ CN NO On <N --< CO p >0 --« 

oi (S cs cn d <s <-! >o Tt t-^ ■^' NO 




^ONOONiOr-H^OONO-^fS 
^ ^ (S '-I 00 '-< -^ >0 CS Tt -rj- ■<;t 


FREQ. 
ASYM 


NO "^ <s >n NO Ti" cs —1 


ACl'. 
THRES 


^•7Z<nZZZ on z 

oo°°^'=tP<»Z^. g. 


FREQ. 
THRES 


Z 
o 


m r~ 




t^Qu^iOfcOfcOCSooa, 


z 

o 

H 

u 

D 


cnOr<-jvnN'>d-_cN'-;<Nprop 
cnro<r)(Ncnu-i<rioN>o-^'Nod 

+ 4- + + + + + +>+> + 

o^o^JJJ^H-ljC5joo'-> 

(N "^^ >0 NO •<* 00 <0 ^ (N NO ^ p 

ddd^cS'-<d'-<dNddrji 
11 II II II II II II II II II II II 

J J J J J J J J J J J J 




(Sr^r-~.^^2^cncn<n(nco 


3 


<N W pj _^ ^ — — 

OnOnOnOnOnOnO\>— II— 1.— II— (,— 1 
OOOOOOOOOOOOOOOvI^ONOnON 

oooooooooooo 
oooooooooooo 




— i(N(NmcoTt-^>ow-)mio>o 



<^ 
< 

'"' en tu 

as 






CV 

(m/sec) 


r^ r- r- 

NO NO NO 

odd 


aS 


ppp «n 
wS >o >n u-i 

(S <N CN 


MRI 
(m/sec) 


<N OO O NO 
I— 1 (N <S CTl 




<S r-; NO NO 

oi en en fo 


FREQ. 
ASYM. 


^zzz 

Tt CN >0 >0 

>ncn inNo 


ACl'. 
THRES 


7.5N/S 
9.1N 

19N 

18N 


FREQ. 
THRES 


Z 

' »— 1 

ON 


H 

CO 


> tin tL, tL, 

UhCoQQ 


z 
o 

p 

u 

z 

e 


LnI = -0.2LnF+ 3.0 
LnI=-1.9LnF + 9.6 
Lnl = -0.84LnF+ 6.6 
Lnl = -0.59LnF+ 5.9 




.— 1 "— ' I— 1 CN 

(-hDhO 


1 

E 


033090T 
033090U 
033090TS 
0509910 




^ ^ ^ (S 



95 



TABLE G-5 

TMJ NOCICEPTOR REACTIVITY IN NORMAL TISSUE 
VERTICAL PLANE 



Test Conditions 


withRF(n=18) 


without RF (n-9) 


code (n= 11) 


no code (n=7) 


code (n=8) 


no code (n=l) 


Dynamic Force 


10 


8 


6 


3 


Force Velocity 


8 


10 


4 


5 


Movement 


5 


10 


2 


3 


Static Force 


3 


12 


1 


4 


Position 


1 


14 





4 


Conduction 
Velocity 


0.4 to 7.5 

m/sec 

(n=4) 


0.75 to 1.5 

m/sec 

(n=2) 




• 


Post-test 

Spontaneous 

Activity 


2 












96 



TABLE G-6 

TMJ NOCICEPTOR REACTIVITY IN NORMAL TISSUE 
HORIZONTAL PLANE 



Test Conditions 


withRF(n=18) 


without RF (n-9) 


code (n=14) 


no code (n=3) 


code (n=l) 


no code (n=4) 


Dynamic Force 


13 


4 





3 


Force Velocity 


7 


9 





3 


Static Force 


5 


11 








Conduction 
Velocity 


2.5 to 3.3 

m/sec 

(n=2) 


0.5 

m/sec 

(n=l) 


• 


• 


Post-test 

Spontaneous 

Activity 


1 












^4 ? ■•-■ - *»< 



t:l: I 



'«i*-S 



■V K V 



m 



; TABLE G-7 

TMJ NOCICEPTOR REACTIVITY 
IN PREVIOUSLY INFLAMED TISSUE 



Test Conditions 


with RF (n=7) 


without RF (n-8) 


code (n=7) 


no code (n=0) 


code (n=6) 


no code (n=2) 


Dynamic Force 


6 





4 


2 


Force Velocity 


6 





5 


2 


Movement 


1 











Static Force 


2 











Position 


1 











Conduction 
Velocity 


0.7m/sec 
(n=l) 


"-,■ :.f. 








Post-test 

Spontaneous 

Activity 















n 



TABLE G-8 

TMJ NOCICEPTOR REACTIVITY 
IN ACUTELY INFLAMED TISSUE 



Test Conditions 


withRF(n=ll) 


' code (n=9) 


acquired coding (n=8) 


Dynaniic Force 


9 


2 


Force Velocity 


4 


4 


Movement 


2 





Static Force 


4 


5 


Position 


1 


1 


Conduction 
Velocity - : 


0.8 to 6.0 

m/sec 

(n=6) 


• 


Post-test 
Spontaneous 

Activity 


• ? ... ■ 


6 



^ .., 



99 



TABLE G-9 

TMJ NOCICEPTOR REACTIVITY 
IN SALINE INJECTED TISSUE 



Test Conditions 


with RF (n=8) 


code (n=7) 


acquired coding (n=l) 


Dynamic Force 


6 





Force Velocity 


2 


1 


Movement 








Static Force 


6 





Position 








Conduction 

Velocity 


0.5-8.5 

m/sec 

(n=2) 


• 


Post-test 

Spontaneous 

Activity 


•■ 






100 



TABLE G- 10 

EFFECT OF CARRAGEENAN IN ACUTELY INFLAMED TISSUE 
REACTIVITY IN THE VERTICAL PLANE 

UNIT#1 





Test Condition 




Pre 


Post 


Post-Pre 




Dynamic Force 


Act. Thres. 


12N 


1.7N 


-10.3N 






Freq. Asymptote 


SON 


69N 


19N 








Mean Rate 


3.4 


2.7 


-0.7 








Slope 


-0.44 


-0.19 


-0.25 








Freq. Thres. 


• 


• 


• 








2 
R 


0.18 


0.44 


0.26 














Static Force 


Act. Thres. 


7N 


1.6 


-5.4N 








Freq. Asymptote 


17N 


30N 


13N 








Mean Rate 


4.5 


5.1 


0.6 








Slope 


-0.4 


-0.68 


-0.28 








Freq. Thres. 

2 
R 


ION 


1.6N 


-8.4N 








0.23 


0.60 


0.42 














Position 


Act. Thres. 


10.5° 


3.4° 


-7.r 








Freq. Asymptote 


16° 


22* 


6.0° 








Mean Rate 


5.2 


3.3 


-1.5 








Slof)e 


-1.1 


-1.2 


-0.1 






. 


Freq. Thres. 


10.0 


2.7° 


-7.3° 








2 
R 


0.35 


0.79 


0.44 














Movement 


Act. Thres. 


9.8° 


6.2° 


-3.6° 








Freq. Asymptote 


14° 


25° 


11° 








Mean Rate 


7.3 


3.13 


-4.13 








Slope 


-4.0 


-0.5 


3.5 






J.^ ^! 


Freq Thres. 

2 
R 


• 


« 










0.6 


0.47 


-0.13 














Force Velocity 


Act. Thres. 




2.0 N/s 










Freq. Asymptote 




317 N/s 








. ; ■ " ^ 


Mean Rate 




2.8 








■ • .* J '» -^'^ 


Slope 

Freq Thres. 

2 
R 




-0.11 












0.35 










" ' 


' 





101 



. *« 



TABLE G- 11 
EFFECT OF CARRAGEENAN IN ACUTELY INFLAMED TISSUE 
REACTIVITY IN THE VERTICAL PLANE 
UNIT #2 



Test Condition 




Pre 


Post 


Post-Pre 


Dynamic Force 


Act. Thres. 
Freq. Asymptote 
Mean Rate 
Slope 
Freq. Thres. 

2 
R 


6.0N 
33N 
4.8 
-0.44 

0.42 


27N 
66N 
3.0 
-0.46 

. 

0.11 


21N 
33N 
-1.8 
0.01 

-0.31 



Movement 


Act. Thres. 


8.0° 


23° 


15° 




Freq. Asymptote 


24° 


28° 


4.0° 




Mean Rate 


4.1 


7.3 


3.2 




Slope 


-0.8 


-2.5 


1.7 




Freq. Thres. 


• 


• 


. 




2 
R 


0.48 


0.19 


-0.29 



Static Force 


Act. Thres. 
Freq. Asymptote 
Me^n Rate 
Slope 
Freq Thres. 

2 
R 




25N 

59N 

3.6 

-1.5 

12.0 

0.62 








102 



TABLE G-12 

EFFECT OF CARRAGEENAN IN ACUTELY INFLAMED TISSUE 
REACTIVITY IN THE VERTICAL PLANE 

UNIT #3 



Test Condition 




Pre 


Post 


Post-Pre 


Dynamic Force 


Act. Thres. 
Freq. Asymptote 
Mean Rate 
Slope 
Freq. Thres. 

2 
R 


26N 

SON 
4.4 
-2.7 

0.50 


40.7N 
76N 
2.8 
-1.17 

0.10 


14.7N 
26N 
-1.6 
-1.5 

-0.40 



Movement 


Act. Thres. 


21° 


24° 


3.0° 




Freq. Asymptote 


26° 


25.5° 


-0.5° 




Mean Rate 


14 


22 


8.0 




Slope 


-7.0 


-7.9 


0.9 




Freq. Thres. 


24° 


26° 


20° 




2 
R 


0.40 


0.90 


0.50 



Force Velocity 

• • 


Act. Thres. 

Freq. Asymptote 

Mean Rate 

Slope 

Freq Thres. 

2 
R 




20.0N/S 
285N/S 
1.9 
-0.4 

0.13 


• 
• 



103 



TABLE G- 13 

EFFECT OF CARRAGEENAN IN ACUTELY INFLAMED TISSUE 
REACTIVITY IN THE VERTICAL PLANE 

UNIT #4 



Test Condition 




Pre 


Post 


Post-Pre 


Dynamic Force 


Act. Thres. 
Freq. Asymptote 
Mean Rate 
Slope 
Freq. Thres. 

2 
R 


17N 

7.5N 

3.8 
-0.6 

0.33 


49N 

23N 
3.7 
-1.0 

0.52 


32N 
15.5N 
-1.1 
0.4 

0.19 



Movement 


Act. Thres. 


18- 


11* 


-7.0- 




Freq. Asymptote 


29- 


20° 


-9.0* 




Mean Rate 


5.3 


4.2 


-LI 


■ J ,- ■-. . ' 


Slope 


-2.1 


-1.7 


-0.4 




Freq. Thres. 


• 


• 


• 




2 
R 


0.32 


0.66 


0.34 



Position 



Act. Thres. 

Freq. Asymptote 

Mean Rate 

Slope 

Freq. Thres. 

2 
R 



20° 

29° 
7.7 
-3.3 

-14.7° 

0.65 



Force Velocity 


Act. Thres. 

Freq. Asymptote 

Mean Rate 

Slope 

Freq Thres. 

2 
R 


2.2N/S 
23.5N/S 
3.2 
-0.12 

0.11 









104 

TABLE G- 14 

EFFECT OF CARRAGEENAN IN ACUTELY INFLAMED TISSUE 
REACTIVITY IN THE HORIZONTAL PLANE 

UNIT #1 






Test Condition 




Pre 


Post 


Post-Pre 






Dynamic Force 


Act. Thres. 
Freq. Asymptote 
Mean Rate 
Slope 
Freq. Thres. 

2 
R 


• 


1.4N 
34N 

4.1 
-0.6 

0.45 










Force Velocity 


Act. Thres. 

Freq. Asymptote 

Mean Rate 

Slope 

Freq. Thres. 

2 
R 




3.0N/S 
132N/S 
3.9 
-0.08 

0.12 










Static Force 


Act. Thres. 

Freq. Asymptote 

Mean Rate 

Slope 

Freq Thres. 

2 
R 




10.7N 

29N 
4.6 
-0.97 
2.8N 

0.37 






:-] I.W ' ^ ''' ■■ ... ..... .s ' i 'U - - 

.. • ^. ■ - . ** 





105 

■ ■* 

TABLE G-15 

EFFECT OF CARRAGEENAN IN ACUTELY INFLAMED TISSUE 
REACTIVITY IN THE HORIZONTAL PLANE 
UNIT #2 






Test Condition 




Pre 


Post 


Post-Pre 


Dynamic Force 


Act. Thres. 
Freq. Asymptote 
Mean Rate 
Slope 
Freq. Thres. 

2 
R 


2.7N 
30N 

2.0 
-1.1 

0.63 


1.3N 
32N 

3.4 
-0.5 

0.49 


-1.4N 
2.0N 
0.5 

-0.6 

-0.14 








Force Velocity 


Act. Thres. 

Freq. Asymptote 

Mean Rate 

Slope 

Freq. Thres. 

2 
R 


IN/s 
286N/S 
2.5 
-0.26 

0.30 


1.6N/S 
185N/S 
3.5 
-0.17 

0.29 


0.6N/S 
-lOlN/s 
1.0 
-0.09 

• 

-0.01 








Static Force 


Act. Thres. 

Freq. Asymptote 

Mean Rate 

Slope 

Freq Thres. 

2 
R 




3.2N 
30N 

4.2 
-0.6 

2.1N 

0.63 




. ._-■,!.■ ^A-, - .- UJ.'. 







106 



TABLE G- 16 

EFFECT OF CARRAGEENAN IN ACUTELY INFLAMED TISSUE 
REACTIVITY IN THE HORIZONTAL PLANE 
UNIT #3 



Test Condition 




Pre 


Post 


Post-Pre 


Dynamic Force 


Act. Thres. 
Freq. Asymptote 
Mean Rate 
Slope 
Freq. Thres. 

2 
R 


3.0N 
33N 
2.9 
-0.58 

0.53 


6.3N 
13N 
4.0 
-1.0 

0.64 


3.3N 
-20N 
1.1 
1.32 

0.11 



Force Velocity 


Act. Thres. 


IN/s 


13N/S 


12N/S 




Freq. Asymptote 


171N/S 


179N/S 


8N/S 




Mean Rate 


3.1 


2.9 


-0.2 




Slope 


-0.18 


-1.2 


1.38 




Freq. Thres. 

2 
R 


• 




• 




0.38 


0.69 


0.31 



Static Force 


Act. Thres. 




3.9N 






Freq. Asymptote 
Mean Rate 




7.9N 
4.7 






Slope 

Freq Thres. 

2 . ,■ 
R 




-2.0 
2.9N 

0.60 





107 



TABLE G- 17 

EFFECT OF CARRAGEENAN IN ACUTELY INFLAMED TISSUE 
REACTIVITY IN THE HORIZONTAL PLANE 

UNIT #4 



Test Condition 



Dynamic Force 



Act. Thres. 
Freq. Asymptote 
Mean Rate 
Slope 
Freq. Thres. 

2 
R 



Pre 



9.5N 
52N 
3.2 
-0.27 



0.11 



Post 



6.4N 
SON 
3.4 
-0.7 



0.60 



Post-Pre 



-3.1N 
-2.0N 
0.2 
0.43 



0.49 



Force Velocity 


Act. Thres. 


27N/S 


5.0N/S 


-22N/S 




Freq. Asymptote 


333N/S 


155N/S 


-178N/S 




Mean Rate 


2.9 


3.1 


-0.2 




Slope 


-0.34 


-0.25 


-0.09 




Freq. Thres. 


• 


• 


• 




2 
R 


0.39 


0.26 


-0.13 



Static Force 


Act. Thres. 


19N 


18N 


-l.ON 




Freq. Asymptote 


41N 


52N 


UN 




Mean Rate 


4.2 


3.7 


-0.5 




Slope 


-1.04 


-1.5 


0.46 




Freq Thres. 


10.7N 


9.0N 


-1.7N 




2 
R 


0.50 


0.70 


0.20 



108 



TABLE G- 18 

EFFECT OF CARRAGEENAN IN ACUTELY INFLAMED TISSUE 
REACTIVITY IN THE HORIZONTAL PLANE 
UNIT #5 



Test Condition 




Pre 


Post 


Post-Pre 


Dynamic Force 


Act. Thres. 
Freq. Asymptote 
Mean Rate 
Slope 
Freq. Thres. 

2 
R 


13.6N 

17.9N 

4.7 

-4.3 

0.84 


1.4N 
8.8N 
2.5 
-1.5 

0.28 


-12.2N 
-9. IN 
-2.2 
-2.8 

-0.56 



i- r 



\ 



' ^ '■:'■ ■+<" 



.■? -..,'-, 



109 



TABLE G- 19 

EFFECT OF CARRAGEENAN IN ACUTELY INFLAMED TISSUE 
REACTIVITY IN THE HORIZONTAL PLANE 

UNIT #6 



Test Condition 




Pre 


Post 


Post-Pre 


Dynamic Force 


Act. Thres. 
Freq. Asymptote 
Mean Rate 
Slope 
Freq. Thres. 

2 
R 


27N 
58N 
3.5 
-0.88 

0.30 


ION 
34N 

2.9 

-0.34 

0.28 


-17N 
-24N 
-0.6 
0.54 

-0.02 



Static Force 


Act. Thres. 


35N 


6.0N 


-29N 




Freq. Asymptote 


41N 


48N 


7.0N 




Mean Rate 


7.9 


4.6 


-3.3 




Slope 


-1.5 


-0.3 


-1.2 




Freq. Thres. 


4.0N 


5.0N 


l.ON 




2 
R 


0.90 


0.38 


-0.52 



uo 



TABLE G-20 

EFFECT OF CARRAGEENAN IN ACUTELY INFLAMED TISSUE 
REACTIVITY IN THE HORIZONTAL PLANE 
UNIT #7 



Test Condition 




Pre 


Post 


Post-Pre 


Dynamic Force 


Act. Thres. 
Freq. Asymptote 
Mean Rate 
Slope 
Freq. Thres. 

2 
R 




7.9N 
30N 

4.8 
-1.04 

0.58 




^ 


Movement 


Act. Thres. 

Freq. Asymptote 

Me<in Rate 

Slope 

Freq. Thres. 

2 
R 




l.ON/s 
40N/S 

4.6 
-0.32 

0.40 






Force Velocity 


Act. Thres. 

Freq. Asymptote 

Mean Rate 

Slope 

Freq Thres. 

2 
R 




3. IN 
4.3N 
8.3 
-2.7 
3.1N 

0.47 





Ill 



TABLE G-21 

EFFECT OF SALINE 
REACTIVITY IN THE HORIZONTAL PLANE 
UNIT#1 



Test Condition 


. 


Pre 


Post 


Post-Pre 


Dynamic Force 


Act. Thres. 
Freq. Asymptote 
Me^n Rate 
Slope 
Freq. Thres. 

2 
R 


4.3N 
26N 

2.5 
-2.1 

0.77 


6.4N 
35N 

3.2 
-0.74 

0.27 


2.1N 
9.0N 
0.7 
-1.36 

-0.50 



Force Velocity 


Act. Thres. 


7. ON 


5.0N/S 


-2.0N 




Freq. Asymptote 


122N 


154N/S 


13N/S 




Mean Rate 


2.0 


2.6 


0.6 




Slope 


-0.57 


-0.21 


-0.36 




Freq. Thres. 


• 


• 


• 




2 
R 


0.42 


0.31 


-0.11 



Static Force 


Act. Thres. 
Freq. Asymptote 
Mean Rate 


7.1N 
27N 
2.9 


2.8N 
29N 
2.9 


-4.3N 
2.0N 
0.0 




Slope 
Freq Thres. 


-1.5 
7. ON 


-.72 
1.4N 


-0.78 
-5.6N 




2 
R 


0.60 


0.68 


0.08 



112 



TABLE G-22 

EFFECT OF SALINE 
REACTIVITY IN THE HORIZONTAL PLANE 
UNIT #2 



Test Condition 



Dynamic Force 



Act. Thres. 
Freq. Asymptote 
Mean Rate 
Slope 
Freq. Thres. 

2 
R 



Pre 



6.9N 
48N 
3.6 
-0.35 



0.20 



Post 



7. ON 
46 
3.5 
-0.62 



0.59 



Post-Pre 



O.IN 
-2.0N 
-0.1 

0.27 



0.39 



Static Force 


Act. Thres. 


20N 


UN 


-9.0N 




Freq. Asymptote 


49N 


60N 


UN 




Mean Rate 


4.0 


3.1 


-0.9 




Slope 


-1.4 


-0.99 


-0.42 




Freq. Thres. 


• 


9.0N 


-5.0N 




2 
R 


0.66 


0.52 


-0.14 



Force Velocity 


Act. Thres. 
Freq. Asymptote 
Mean Rate 
Slope 
Freq Thres. 

2 
R 




13N/S 

179N/9 

3.3 

-0.4 

0.63 





,.■ .f' 



«>■«» 



^„>^; r '", c'-'-i 



113 



TABLE G-23 

* EFFECT OF SALINE 
REACTIVITY IN THE HORIZONTAL PLANE 
UNIT #3 



Test Condition 



Dynamic Force 



Act. Thres. 
Freq. Asymptote 
Mean Rate 
Slope 
Freq. Thres. 

2 
R 



Pre 



13N 
49N 
3.5 
-0.74 



0.45 



Post 



15N 
28N 

3.5 

-0.83 



0.28 



Post-Pre 



2.0N 
-21N 
0.0 
0.09 



-0.11 



Static Force 


Act. Thres. 


UN 


7. ON 


-4.0N 




Freq. Asymptote 


38N 


41N 


3.0N 




Mean Rate 


3.75 


3.71 


-0.04 


:. 


Slope 


-0.53 


-0.48 


-0.05 




Freq. Thres. 


8.0N 


6.0N 


-2.0N 




2 
R 


0.36 


0.28 


-0.08 



114 



TABLE G-24 

EFFECT OF SALINE 
REACTIVITY IN THE VERTICAL PLANE 

UNIT #4 



Test Condition 


., :■*'■'■ 


Pre 


Post 


Post-Pre 


Dynamic Force 


Act. Thres. 
Freq. Asymptote 
Mean Rate 
Slope 
Freq. Thres. 

2 
R 


5.7N 
54N 

3.2 
-0.55 

0.53 








Force Velocity 


Act. Thres. 

Freq. Asymptote 

Mean Rate 

Slope 

Freq. Thres. 

2 
R 


UN 

257N 

3.1 

-0.3 

0.51 








Movement 


Act. Thres. 

Freq. Asymptote 

Mean Rate 

Slope 

Freq. Thres. 

2 
R 


9.9° 
25° 

3.9 
-1.5 

0.58 








Static Force 


Act. Thres. 

Freq. Asymptote 

Mean Rate 

Slope 

Freq Thres. 

2 
R 


6.4N 
50N 

3.4 
-0.8 
3.0N 

0.65 







Position 


Act. Thres. 

Freq. Asymptote 

Mean Rate 

Slope 

Freq Thres. 

2 
R 


15° 

25° 
5.6 
-0.32 
9.0° 

0.62 







115 



TABLE G-25 

EFFECT OF SALINE 
REACTIVITY IN THE HORIZONTAL PLANE 

UNIT #6 



Test Condition 




Pre 


Post 


Post-Pre 


Dynamic Force 
ft 


Act. Thres. 
Freq. Asymptote 
Mean Rate 
Slope 
Freq. Thres. 

2 . s. , 
R 


46N 

71N 
5.5 
-1.7 

0.37 


25N 

59N 
4.2 
-1.2 

0.43 


-21N 
-12N 
-1.3 
-0.05 

-0.06 



f " 



116 



TABLE G-26 

EFFECT OF SALI^fE 
REACTIVITY IN THE HORIZONTAL PLANE 
UNIT #7 



Test Condition 




Pre 


Post 


Post-Pre 


Dynamic Force 


Act. Thres. 
Freq. Asymptote 
Mean Rate 
Slope 
Freq. Thres. 

2 
R 


7.4N 
59N 
3.6 
-0.54 

0.32 


UN 

68N 
3.8 
-0.27 

0.20 


3.6N 
9.0N 
0.2 
-0.27 

-0.12 



Static Force 



Act. Thres. 

Freq. Asymptote 

Mean Rate 

Slope 

Freq. Thres. 

2 
R 



UN 


8.6N 


-2.4N 


60N 


60N 


O.ON 


3.3 


3.9 


0.6 


-1.30 


-0.53 


-0.77 


5.0N 


6.0N 


l.ON 


0.77 


0.60 


-0.17 



fi 



• -- ' > \ » 



117 



TABLE G-27 

EFFECT OF SALINE 
REACTIVITY IN THE HORIZONTAL PLANE 
UNIT #8 , 



Test Condition 



Dynamic Force 



Act. Thres. 
Freq. Asymptote 
Mean Rate 
Slope 
Freq. Thres. 

2 
R 



Pre 



7.0N 
48N 
3.3 
-0.78 



0.37 



Post 



Post-Pre 



5.0N 

56N 
3.2 
-0.86 



0.73 



-2.0N 
8.0N 
-0.1 
0.08 



0.36 



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BIOGRAPHICAL SKETCH 

I was bom on December 13, 1943, in Greensburg, Pennsylvania. I attended 
Pennsylvania State University between 1961 and 1965 where I received a Bachelor of 
Science degree in biochemistry. I attended New York University between 1965 and 1969 
where I received a Doctor of Dental Surgery degree in dentistry. In 1985 and 1986, I 
attended the University of Florida as a postgraduate fellow in the Facial Pain Center of the 
dental school. I received a Masters of Anatomy degree in the Department of Anatomy and 
Cell Biology, University of Florida between 1986 and .1987. I pursued a Doctor of 
Philosophy degree in the Department of Oral Biology, University of Florida, between 1987 
and 1992, and will graduate in May, 1992. 



130 



I certify that I have read this study and that in my opinion it conforms to acceptable 
standards of scholarly presentation and is fully adequate, in scope and quality, as a 
dissertation for the degree of Doctor of Philosophy. 




Parker MahanTUnairman 
Distinguished Service Professor 
of Oral Biology 



I certify that I have read this study and that in my opinion it conforms to acceptable 
standards of scholarly presentation and is fully adequate, in scope and quality, as a 
dissertation for the degree of Doctor of Philosophy. 




Brian Cooper, Gochairman 
Assistant Professor of Neuroscience 



I certify that I have read this study and that in my opinion it conforms to acceptable 
standards of scholarly presentation and is fully adequate, in scope and quality, as a 
dissertation for the degree of Doctor of Philosophy. 




(^.M^ 



iology 



I certify that I have read this study and that in my opinion it conforms to acceptable 
standards of scholarly presentation and is fully adequate, in scope and quality, as a; 
dissertation for the degree of Doctor of Philosophy. 




Vier^„ 

Professor of Neuroscience 






t.;.i ? 



'"♦■' : F ■ ,.i 



I certify that I have read this study and that in my opinion it conforms to acceptable 
standards of scholarly presentation and is fully adequate, in scope and quality, as a 
dissertation for the degree of Doctor of Philosophy. 



;< 




Lynn^larkin 

lessor of Anatomy 
and Cell Biology 



This dissertation was submitted to the Graduate Faculty of the College of Medicine 
and to the Graduate School and was accepted as partial fulfillment of the requirements for 
the degree of Doctor of Philosophy. 



May 1992 




Dean, College of Medicine 



Dean, Graduate School 



UNIVERSITY OF FLORIDA 



3 1262 08554 7213 



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